Physiological costs of chemical defence: repeated reflex bleeding weakens the immune system and postpones reproduction in a ladybird beetle

Cuénot, L. Sur la saignée réflexe et les moyens défense de quelques insectes. Arch. Zool. Exp. Gen. 4, 655–680 (1896).

Google Scholar 

Hollande, C. H. L’autohémorrhée ou le rejet du sang chez les insectes (toxicologie du sang). Archs. Anal. Microsc. 13, 171–318 (1911).

Google Scholar 

Bateman, P. W. & Fleming, P. A. There will be blood: autohaemorrhage behaviour as part of the defence repertoire of an insect. Journal of Zoology 278, 342–348, https://doi.org/10.1111/j.1469-7998.2009.00582.x (2009).

Article  Google Scholar 

Bugila, A. A. A., Franco, J. C., da Silva, E. B. & Branco, M. Defense Response of Native and Alien Mealybugs (Hemiptera: Pseudococcidae) Against the Solitary Parasitoid Anagyrus sp nr. pseudococci (Girault) (Hymenoptera: Encyrtidae). Journal of Insect Behavior 27, 439–453, https://doi.org/10.1007/s10905-014-9440-x (2014).

Article  Google Scholar 

Moore, K. A. & Williams, D. D. Novel Strategies in the Complex Defense Repertoire of a Stonefly (Pteronarcys Dorsata) Nymph. Oikos 57, 49–56, https://doi.org/10.2307/3565735 (1990).

Article  Google Scholar 

Drilling, K. & Dettner, K. First insights into the chemical defensive system of the erotylid beetle, Tritoma bipustulata. Chemoecology 20, 243–253, https://doi.org/10.1007/s00049-010-0054-2 (2010).

CAS  Article  Google Scholar 

Fu, X. H., Nobuyoshi, O., Meyer-Rochow, V. B., Wang, Y. Y. & Lei, C. L. Reflex-bleeding in the firefly Pyrocoelia pectoralis (Coleoptera: Lampyridae): Morphological basis and possible function. Coleopterists Bulletin 60, 207–215, https://doi.org/10.1649/892.1 (2006).

Article  Google Scholar 

Nicolson, S. W. Water Replenishment Following Reflex Bleeding in the Blister Beetle Decapotoma-Lunata Pallas (Coleoptera, Meloidae). African Entomology 2, 21–23 (1994).

Google Scholar 

Sato, S., Kushibuchi, K. & Yasuda, H. Effect of reflex bleeding of a predatory ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), as a means of avoiding intraguild predation and its cost. Applied Entomology and Zoology 44, 203–206, https://doi.org/10.1303/aez.2009.203 (2009).

Article  Google Scholar 

Boevé, J.-L. & Schaffner, U. Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134, 104–111, https://doi.org/10.1007/s00442-002-1092-4 (2003).

ADS  Article  PubMed  Google Scholar 

Higginson, A. D., Delf, J., Ruxton, G. D. & Speed, M. P. Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae. Journal of Animal Ecology 80, 384–392, https://doi.org/10.1111/j.1365-2656.2010.01786.x (2011).

Article  PubMed  Google Scholar 

Sword, G. A. Tasty on the outside, but toxic in the middle: grasshopper regurgitation and host plant-mediated toxicity to a vertebrate predator. Oecologia 128, 416–421, https://doi.org/10.1007/s004420100666 (2001).

ADS  Article  PubMed  Google Scholar 

Novgorodova, T. A. Role of social and individual experience in interaction of the meadow ant Formica pratensis (Hymenoptera: Formicidae) with ladybird imagines and hoverfly larvae. Insect Science 22, 440–450, https://doi.org/10.1111/1744-7917.12127 (2015).

Article  PubMed  Google Scholar 

Zvereva, E. L. & Kozlov, M. V. The costs and effectiveness of chemical defenses in herbivorous insects: a meta-analysis. Ecological Monographs 86, 107–124, https://doi.org/10.1890/15-0911.1 (2016).

Article  Google Scholar 

Eisner, T., Eisner, M. & Siegler, M. V. S. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. (Harvard University Press, 2005).

Holloway, G. J., de Jong, P. W., Brakefield, P. M. & de Vos, H. Chemical defence in ladybird beetles (Coccinellidae). 1. Distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinella septempunctata). Chemoecology 2, 7–14 (1991).

CAS  Article  Google Scholar 

Karystinou, A., Thomas, A. P. M. & Roy, H. E. Presence of haemocyte-like cells in coccinellid reflex blood. Physiological Entomology 29, 94–96, https://doi.org/10.1111/j.0307-6962.2004.0358.x (2004).

Article  Google Scholar 

Knapp, M., Dobes, P., Rericha, M. & Hyrsl, P. Puncture vs. reflex bleeding: Haemolymph composition reveals significant differences among ladybird species (Coleoptera: Coccinellidae), but not between sampling methods. European Journal of Entomology 115, 1–6, https://doi.org/10.14411/eje.2018.001 (2018).

Article  Google Scholar 

Grill, C. P. & Moore, A. J. Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114, 274–282, https://doi.org/10.1007/s004420050446 (1998).

ADS  Article  PubMed  Google Scholar 

Rowell-Rahier, M. & Pasteels, J. M. Economics of Chemical Defense in Chrysomelinae. Journal of Chemical Ecology 12, 1189–1203, https://doi.org/10.1007/bf01639004 (1986).

CAS  Article  PubMed  Google Scholar 

Holloway, G. J., Dejong, P. W. & Ottenheim, M. The Genetics and Cost of Chemical Defense in the 2-Spot Ladybird (Adalia-Bipunctata L). Evolution 47, 1229–1239, https://doi.org/10.2307/2409988 (1993).

Article  PubMed  Google Scholar 

Lee, B. W., Ugine, T. A. & Losey, J. E. An Assessment of the Physiological Costs of Autogenous Defenses in Native and Introduced Lady Beetles. Environmental Entomology 47, 1030–1038, https://doi.org/10.1093/ee/nvy068 (2018).

CAS  Article  PubMed  Google Scholar 

Rericha, M., Dobes, P., Hyrsl, P. & Knapp, M. Ontogeny of protein concentration, haemocyte concentration and antimicrobial activity against Escherichia coli in haemolymph of the invasive harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Physiological Entomology 43, 51–59, https://doi.org/10.1111/phen.12224 (2018).

CAS  Article  Google Scholar 

de Jong, P. W., Holloway, G. J., Brakefield, P. M. & de Vos, H. Chemical defence in ladybird beetles (Coccinellidae). II. Amount of reflex fluid, the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adalia bipunctata). Chemoecology 2, 15–19 (1991).

Article  Google Scholar 

Schmidtberg, H., Roehrich, C., Vogel, H. & Vilcinskas, A. A switch from constitutive chemical defence to inducible innate immune responses in the invasive ladybird Harmonia axyridis. Biology Letters 9, 20130006, https://doi.org/10.1098/rsbl.2013.0006 (2013).

Article  PubMed  PubMed Central  Google Scholar 

Firlej, A., Girard, P.-A., Brehelin, M., Coderre, D. & Boivin, G. Immune Response of Harmonia axyridis (Coleoptera: Coccinellidae) Supports the Enemy Release Hypothesis in North America. Annals of the Entomological Society of America 105, 328–338, https://doi.org/10.1603/an11026 (2012).

Article  Google Scholar 

Vilcinskas, A., Mukherjee, K. & Vogel, H. Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proceedings of the Royal Society B-Biological Sciences 280, 20122113, https://doi.org/10.1098/rspb.2012.2113 (2013).

CAS  Article  PubMed Central  Google Scholar 

Yang, S. Y., Ruuhola, T. & Rantala, M. J. Impact of starvation on immune defense and other life-history traits of an outbreaking geometrid, Epirrita autumnata: a possible causal trigger for the crash phase of population cycle. Annales Zoologici Fennici 44, 89–96 (2007).

Google Scholar 

Boggs, C. L. Understanding insect life histories and senescence through a resource allocation lens. Functional Ecology 23, 27–37, https://doi.org/10.1111/j.1365-2435.2009.01527.x (2009).

Article  Google Scholar 

Povey, S., Cotter, S. C., Simpson, S. J., Lee, K. P. & Wilson, K. Can the protein costs of bacterial resistance be offset by altered feeding behaviour? Journal of Animal Ecology 78, 437–446, https://doi.org/10.1111/j.1365-2656.2008.01499.x (2009).

Article  PubMed  Google Scholar 

Simpson, S. J. & Raubenheimer, D. The Central Role of the Hemolymph in the Regulation of Nutrient Intake in Insects. Physiological Entomology 18, 395–403 (1993).

CAS  Article  Google Scholar 

Hodek, I., Honěk, A. & van Emden, H. F. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). 600 (Willey-Blackwell, 2012).

Knapp, M. Relative Importance of Sex, Pre-Starvation Body Mass and Structural Body Size in the Determination of Exceptional Starvation Resistance of Anchomenus dorsalis (Coleoptera: Carabidae). Plos One 11, e0151459, https://doi.org/10.1371/journal.pone.0151459 (2016).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Chown, S. L., Le Lagadec, M. D. & Scholtz, C. H. Partitioning variance in a physiological trait: desiccation resistance in keratin beetles (Coleoptera, Trogidae). Functional Ecology 13, 838–844, https://doi.org/10.1046/j.1365-2435.1999.00373.x (1999).

Article  Google Scholar 

Bayoumy, M. H., Osawa, N. & Hatt, S. Fitness costs of reflex bleeding in the ladybird beetle Harmonia axyridis: the role of parental effects. Insect Science in press, https://doi.org/10.1111/1744-7917.12737 (2020).

Brown, P. M. J. et al. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53, 5–21, https://doi.org/10.1007/s10526-007-9132-y (2008).

Article  Google Scholar 

Brown, P. M. J. et al. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56, 623–641, https://doi.org/10.1007/s10526-011-9379-1 (2011).

Article  Google Scholar 

Lombaert, E. et al. Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird. Plos One 5, e9743, https://doi.org/10.1371/journal.pone.0009743 (2010).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Tayeh, A. et al. Biological invasion and biological control select for different life histories. Nature Communications 6, 7268, https://doi.org/10.1038/ncomms8268 (2015).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

R Development Core Team. R: A language and environment for statistical computing., (R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org, 2018).