Bombardiers and assassins: mimetic interactions between unequally defended insects

Akino K, Sasaki M, Okamoto D. 1956. Studies on mole-crickets attacking rice seeds

directly sown without transplanting between rows of wheat and barley. Bulletin of

the Chugoku National Agricultural Experiment Station 3(1):91–110 (in Japanese with

English résumé).

Alvarez LJ, Zamudio F, Melo MC. 2019. Eating with the enemy? Mimic complex

between a stingless bee and assassin bugs. Papéis Avulsos de Zoologia 59:e20195927

DOI 10.11606/1807-0205/2019.59.27.

Aneshansley DT, Eisner T, Widom JM, Widom B. 1969. Biochemistry at 100 ◦ C: explosive secretory discharge of bombardier beetles (Brachinus). Science 165(3888):61–63

DOI 10.1126/science.165.3888.61.

Anichtchenko A, Choi JB, Facchini S, Marrero J, Panin R, Potanin D, Roguet D,

Solodovnikov I, Will KW. 2022. Carabidae of the World. Available at https://

carabidae.org/taxa/licinini-bonelli (accessed on 23 February 2022).

Arndt EM, Moore W, Lee WK, Ortiz C. 2015. Mechanistic origins of bombardier

beetle (Brachinini) explosion-induced defensive spray pulsation. Science

348(6234):563–567 DOI 10.1126/science.1261166.

Aubier TG, Joron M, Sherratt TN. 2017. Mimicry among unequally defended prey

should be mutualistic when predators sample optimally. The American Naturalist

189(3):267–282 DOI 10.1086/690121.

Balogh ACV, Gamberale-Stille G, Leimar O. 2008. Learning and the mimicry spectrum: from quasi-Bates to super-Müller. Animal Behaviour 76(5):1591–1599

DOI 10.1016/j.anbehav.2008.07.017.

Bates HW. 1862. Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae. Transactions of the Linnean Society of London 23:495–566

DOI 10.1111/j.1096-3642.1860.tb00146.x.

Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using

lme4. Journal of Statistical Software 67:1–48 DOI 10.18637/jss.v067.i01.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

19/26

Bonacci T, Aloise G, Brandmayr P, Brandmayr TZ, Capula M. 2008. Testing the predatory behaviour of Podarcis sicula (Reptilia: Lacertidae) towards aposematic and nonaposematic preys. Amphibia-Reptilia 29:449–453 DOI 10.1163/156853808785111986.

Bonacci T, Brandmayr P, Brandmayr TZ. 2011. Predator feeding choice on conspicuous and non-conspicuous carabid beetles: first results. ZooKeys 100:171–179

DOI 10.3897/zookeys.100.1525.

Chatelain P, Elias M, Fontaine C, Villemant C, Dajoz I, Perrard A. 2023. Müllerian

mimicry among bees and wasps: a review of current knowledge and future avenues

of research. Biological Reviews DOI 10.1111/brv.12955.

Chłond D. 2018. A taxonomic revision of the genus Sirthenea (Hemiptera: Heteroptera:

Reduviidae) of the Old World. Zootaxa 4520(1):1–85

DOI 10.11646/zootaxa.4520.1.1.

Chłond D, Bugaj-Nawrocka A, Sawka-Gądek N. 2019. Are we witnessing speciation? A

case study of the species Sirthenea flavipes (Stål, 1855) (Heteroptera: Reduviidae).

Austral Entomology 58(1):96–110 DOI 10.1111/aen.12320.

Chouteau M, Dezeure J, Sherratt TN, Llaurens V, Joron M. 2019. Similar predator

aversion for natural prey with diverse toxicity levels. Animal Behaviour 153:49–59

DOI 10.1016/j.anbehav.2019.04.017.

Dean J. 1979. Defensive reaction time of bombardier beetles: an investigation of

the speed of a chemical defense. Journal of Chemical Ecology 5(5):691–701

DOI 10.1007/BF00986554.

Dean J. 1980. Encounters between bombardier beetles and two species of toads (Bufo

americanus, B. marinus): speed of prey-capture does not determine success. Journal

of Comparative Physiology 135(1):41–50 DOI 10.1007/BF00660180.

Edmunds M. 1974. Defense in animals. Harlow: Longman.

Eisner T. 1958. The protective role of the spray mechanism of the bombardier

beetle, Brachynus ballistarius Lec. Journal of Insect Physiology 2(3):215–220

DOI 10.1016/0022-1910(58)90006-4.

Eisner T, Aneshansley DJ, Campo MLdel, Eisner M, Frank JH, Deyrup M. 2006.

Effect of bombardier beetle spray on a wolf spider: repellency and leg autotomy.

Chemoecology 16(4):185–189 DOI 10.1007/s00049-006-0346-8.

Eisner T, Dean J. 1976. Ploy and counterploy in predator–prey interactions: orb-weaving

spiders versus bombardier beetles. Proceedings of the National Academy of Sciences of

the United States of America 73(4):1365–1367 DOI 10.1073/pnas.73.4.1365.

Eisner T, Eisner M, Siegler M. 2005. Secret weapons: defenses of insects, spiders, scorpions,

and other many-legged creatures. Cambridge: The Belknap Press of the Harvard

University Press.

Eisner T, Meinwald J. 1966. Defensive secretions of arthropods. Science 153(1734):1341–1350

DOI 10.1126/science.153.3742.1341.

Endler JA. 1991. Interactions between predators and prey. In: Krebs JR, Davies NB,

eds. Behavioural ecology: an evolutionary approach. London, Paris, Berlin, Vienna:

Blackwell, 169–196.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

20/26

Fedorenko DN. 2021. Stenaptinus (Coleoptera: Carabidae: Brachininae) of Vietnam.

Note 3. Russian Entomological Journal 30(3):252–263 DOI 10.15298/rusentj.30.3.02.

Forero D, Giraldo-Echeverry NG. 2015. First record of the assassin bug genus Coilopus

Elkins, 1969 (Hemiptera: Heteroptera: Reduviidae) from Colombia. Check List

11(3):1634 DOI 10.15560/11.3.1634.

Fujisawa T, Lee CM, Ishii M. 2012. Species diversity of ground beetle assemblages

in the distinctive landscapes of the Yodo River flowing through northern Osaka

Prefecture, central Japan. Japanese Journal of Environmental Entomology and Zoology

23(2):89–100 DOI 10.11257/jjeez.23.89.

Gil-Santana HR. 2008. New records, and nomenclatural and biological notes on Reduviidae (Hemiptera: Heteroptera) from Bolivia and Brazil. Zootaxa 1785(1):43–53

DOI 10.11646/zootaxa.1785.1.2.

Gil-Santana HR, Forero D, Weirauch C. 2015. Assassin bugs (Reduviidae excluding Triatominae). In: Pannizi AR, Grazia J, eds. True Bugs (Heteroptera) of the

Neotropics. Dordrecht, Heidelberg, New York, London: Springer, 307–351

DOI 10.1007/978-94-017-9861-7_12.

Habu A, Sadanaga K. 1965. Illustrations for identification of larvae of the Carabidae

found in cultivated fields and paddy-fields (III). Bulletin of the National Institute

of Agricultural Sciences, Series C: Plant Pathology and Entomology 19:81–216 (in

Japanese with English summary).

Haviland MD. 1931. The Reduviidae of Kartabo Bartica District, British Guiana.

Zoologica 7(5):129–154.

Hayashi M. 2023. Life history of an assassin bug, Sirthenea flavipes (Stål, 1855): laboratory rearing and field observations. Special Bulletin of the Hoshizaki Green Foundation

32:51–62.

Hirai T. 2002. Ontogenetic change in the diet of the pond frog, Rana nigromaculata.

Ecological Research 17(6):639–644 DOI 10.1046/j.1440-1703.2002.00521.x.

Hirai T, Matsui M. 1999. Feeding habits of the pond frog, Rana nigromaculata, inhabiting rice fields in Kyoto, Japan. Copeia 1999(4):940–947 DOI 10.2307/1447969.

Hirashima Y, Morimoto K. 2008. Iconographia insectorum Japonicorum colore naturali

edita III. Tokyo: Hokuryukan(in Japanese).

Honma A, Oku S, Nishida T. 2006. Adaptive significance of death feigning posture as a

specialized inducible defence against gape-limited predators. Proceedings of the Royal

Society B 273(1594):1631–1636 DOI 10.1098/rspb.2006.3501.

Honma A, Takakura K, Nishida T. 2008. Optimal-foraging predator favors commensalistic Batesian mimicry. PLOS ONE 3(10):e3411 DOI 10.1371/journal.pone.0003411.

Hudson WG. 1987. Ontogeny of prey selection in Sirthenea carinata: generalist juveniles

become specialist adults. Entomophaga 32(4):399–406 DOI 10.1007/BF02372449.

Ihalainen E, Lindström L, Mappes J. 2007. Investigating Müllerian mimicry: predator learning and variation in prey defences. Journal of Evolutionary Biology

20(2):780–791 DOI 10.1111/j.1420-9101.2006.01234.x.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

21/26

Ihalainen E, Lindström L, Mappes J, Puolakkainen S. 2008. Butterfly effects in mimicry?

Combining signal and taste can twist the relationship of Müllerian co-mimics. Behavioral Ecology and Sociobiology 62(8):1267–1276 DOI 10.1007/s00265-008-0555-y.

Ishitani M, Yano K. 1994. Species composition and seasonal activities of ground beetles

(Coleoptera) in a fig orchard. Japanese Journal of Entomology 62(1):201–210.

Ito F, Taniguchi K, Billen J. 2016. Defensive function of petiole spines in queens and

workers of the formicine ant Polyrhachis lamellidens (Hymenoptera: Formicidae)

against an ant predator, the Japanese tree frog Hyla japonica. Asian Myrmecology

8:81–86 DOI 10.20362/am.008014.

Ito S, Okutani T, Hiura I. 1977. Colored illustrations of the insect of Japan II. Osaka:

Hoikusha (in Japanese).

Jackson JF. 1973. Mimicry of Trigona bees by a reduviid (Hemiptera) from British

Honduras. The Florida Entomologist 56(3):200–202 DOI 10.2307/3493124.

Kanehisa K. 1996. Secretion of defensive substance by Carabidae and Brachinidae.

Bulletin of the Research Institute for Bioresources, Okayama University 4(1):9–23 (in

Japanese with English summary).

Kanehisa K, Murase M. 1977. Comparative study of the pygidial defensive systems of carabid beetles. Applied Entomology and Zoology 12(3):225–235

DOI 10.1303/aez.12.225.

Kojima W, Yamamoto R. 2020. Defense of bombardier beetles against avian predators.

The Science of Nature 107:36 DOI 10.1007/s00114-020-01692-z.

Komaki S, Igawa T, Lin SM, Tojo K, Min MS, Sumida M. 2015. Robust molecular

phylogeny and palaeodistribution modelling resolve a complex evolutionary history:

glacial cycling drove recurrent mtDNA introgression among Pelophylax frogs in East

Asia. Journal of Biogeography 42(11):2159–2171 DOI 10.1111/jbi.12584.

Kunte K, Kizhakke AG, Nawge V. 2021. Evolution of mimicry rings as a window

into community dynamics. Annual Review of Ecology, Evolution, and Systematics

52:315–341 DOI 10.1146/annurev-ecolsys-012021-024616.

Lindström L, Lyytinen A, Mappes J, Ojala K. 2006. Relative importance of taste and

visual appearance for predator education in Müllerian mimicry. Animal Behaviour

72(2):323–333 DOI 10.1016/j.anbehav.2005.10.015.

Linsley EG, Esiner T, Klots AB. 1961. Mimetic assemblages of sibling species of lycid

beetles. Evolution 15(1):15–29 DOI 10.1111/j.1558-5646.1961.tb03126.x.

Louis D. 1974. Biology of Reduviidae of cocoa farms in Ghana. The American Midland

Naturalist 91(1):68–89 DOI 10.2307/2424512.

Maldonado Capriles J, Lozada Robles PW. 1992. Key to the group of neotropical waspmimetic harpactorine genera and the description of a new species (Hemiptera:

Reduviidae). Proceedings of the Entomological Society of Washington 94(1):162–165.

Marples NM. 1993. Toxicity assays of ladybirds using natural predators. Chemoecology

4(1):33–38 DOI 10.1007/BF01245894.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

22/26

Marples NM, Brakefield PM, Cowie RJ. 1989. Differences between the 7-spot and 2-spot

ladybird beetles (Coccinellidae) in their toxic effects on a bird predator. Ecological

Entomology 14(1):79–84 DOI 10.1111/j.1365-2311.1989.tb00756.x.

Matsubara S, Sugiura S. 2017. Chemical defence of turnip sawfly larvae against Japanese

tree frogs. Journal of Asia-Pacific Entomology 20(1):225–227

DOI 10.1016/j.aspen.2017.01.001.

Matsui M, Maeda N. 2018. Encyclopedia of Japanese frogs. Tokyo: Bun-ichi Sogo

Shuppan.

Müller F. 1878. Über die vortheile der mimicry bei schmetterlingen. Zoologischer Anzeiger

1:54–55.

Müller F. 1879. Ituna and Thyridia: a remarkable case of mimicry in butterflies. Transactions of the Entomological Society of London 1879:20–29.

Ohwaki A, Kaneko Y, Ikeda H. 2015. Seasonal variability in the response of ground

beetles (Coleoptera: Carabidae) to a forest edge in a heterogeneous agricultural landscape in Japan. European Journal of Entomology 112(1):135–144

DOI 10.14411/eje.2015.022.

Pekár S, Petráková L, Bulbert MW, Whiting MJ, Herberstein ME. 2017. The golden

mimicry complex uses a wide spectrum of defence to deter a community of predators. eLife 6:e22089 DOI 10.7554/eLife.22089.

R Core Team. 2018. R, a language and environment for statistical computing. Vienna: R

Foundation for Statistical Computing.

Raška J, Krajíček J, Bosáková Z, Štys P, Exnerová A. 2020. Larvae of pyrrhocorid true

bugs are not to spiders’ taste: putative Müllerian mimicry. Biological Journal of the

Linnean Society 129(1):199–212 DOI 10.1093/biolinnean/blz174.

Readio PA. 1927. Studies on the biology of the Reduviidae of America North of Mexico.

The University of Kansas Science Bulletin 17(1):5–291.

Rowland HM, Ihalainen E, Lindström L, Mappes J, Speed MP. 2007. Co-mimics have

a mutualistic relationship despite unequal defences. Nature 448(7149):64–67

DOI 10.1038/nature05899.

Rowland HM, Mappes J, Ruxton GD, Speed MP. 2010. Mimicry between unequally

defended prey can be parasitic: evidence for quasi-Batesian mimicry. Ecology Letters

13(12):1494–1502 DOI 10.1111/j.1461-0248.2010.01539.x.

Ruxton GD, Franks DW, Balogh ACV, Leimar O. 2008. Evolutionary implications of

the form of predator generalization for aposematic signals and mimicry in prey.

Evolution 62(11):2913–2921 DOI 10.1111/j.1558-5646.2008.00485.x.

Ruxton GD, Sherratt TN, Speed MP. 2004. Avoiding attack: the evolutionary ecology of

crypsis, aposematism, and mimicry. Oxford: Oxford University Press.

Sano M, Shinohara M. 2012. Species comparison of frogs food habits during mating

seasons in Uenohara, Yamanashi Pref. Japan. Bulletin of Teikyo University of Science

and Technology 8:101–111 (in Japanese with English summary).

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

23/26

Sarashina M, Yoshihisa Y, Yoshida T. 2011. Stomach contents of invasive Black-spotted

Pond frog (Rana nigromaculata) in urban landscape of Sapporo City. Journal of

Rakuno Gakuen University 36(1):81–86 (in Japanese with English summary).

Schaller JC, Davidowitz G, Papaj DR, Smith RL, Carrière Y, Moore W. 2018. Molecular

phylogeny, ecology and multispecies aggregation behaviour of bombardier beetles in

Arizona. PLOS ONE 13(10):e0205192 DOI 10.1371/journal.pone.0205192.

Schmidt JO. 2009. Defensive behavior. In: Resh VH, Cardé RT, eds. Encyclopedia of

Insects. Second Edition. Burlington, San Diego, London: Elsevier, 252–257.

Shelford MA. 1902. Observations on some mimetic insects and spiders from Borneo and

Singapore. Proceedings of the Zoological Society of London 2:230–284.

Sherratt TN. 2008. The evolution of Müllerian mimicry. Naturwissenschaften

95(8):681–695 DOI 10.1007/s00114-008-0403-y.

Shinohara T, Takami Y. 2020. Functional diversity and trade-offs in divergent antipredator morphologies in herbivorous insects. Ecology and Evolution 10(11):5089–5096

DOI 10.1002/ece3.6262.

Skelhorn J, Rowe C. 2006. Taste-rejection by predators and the evolution of unpalatability in prey. Behavioral Ecology and Sociobiology 60(4):550–555

DOI 10.1007/s00265-006-0199-8.

Soukupová TS, Veselý P, Fuchs R. 2021. Wariness to colour patterns: birds versus European red-and-black insects. Ecological Entomology 46(5):1157–1164

DOI 10.1111/een.13060.

Speed MP. 1993. Muellerian mimicry and psychology of predation. Animal Behaviour

45(3):571–580 DOI 10.1006/anbe.1993.1067.

Speed MP. 1999. Batesian, quasi-Batesian or Müllerian mimicry? Theory and data in

mimicry research. Evolutionary Ecology 13(7–8):755–776

DOI 10.1023/A:1010871106763.

Speed MP, Alderson NJ, Hardman C, Ruxton GD. 2000. Testing Müllerian mimicry:

an experiment with wild birds. Proceedings of the Royal Society of London B

267(1444):725–731 DOI 10.1098/rspb.2000.1063.

Speed MP, Turner JRG. 1999. Learning and memory in mimicry: II. Do we understand

the mimicry spectrum? Biological Journal of the Linnean Society 67(3):281–312

DOI 10.1111/j.1095-8312.1999.tb01935.x.

Staddon BW. 1979. The scent glands of Heteroptera. Advances in Insect Physiology

14:351–418 DOI 10.1016/S0065-2806(08)60055-7.

Sugiura S. 2018. Anti-predator defences of a bombardier beetle: is bombing essential for

successful escape from frogs? PeerJ 6:e5942 DOI 10.7717/peerj.5942.

Sugiura S. 2020a. Predators as drivers of insect defenses. Entomological Science

23(3):316–337 DOI 10.1111/ens.12423.

Sugiura S. 2020b. Active escape of prey from predator vent via the digestive tract. Current

Biology 30(15):R867–R868 DOI 10.1016/j.cub.2020.06.026.

Sugiura S. 2021. Beetle bombing always deters praying mantises. PeerJ 9:e11657

DOI 10.7717/peerj.11657.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

24/26

Sugiura S, Date T. 2022. Bombardier beetles repel invasive bullfrogs. PeerJ 10:e13805

DOI 10.7717/peerj.13805.

Sugiura S, Sato T. 2018. Successful escape of bombardier beetles from predator digestive

systems. Biology Letters 14(2):20170647 DOI 10.1098/rsbl.2017.0647.

Sugiura S, Tsujii M. 2022. Male wasp genitalia as an anti-predator defense. Current

Biology 32(24):R1336–R1337 DOI 10.1016/j.cub.2022.11.030.

Takahashi T. 1996. Reduviidae and Nabidae in Hyogo Prefecture (2). Parnassius 43:3–10

(in Japanese).

Takara T. 1957. Provisional list of Hemiptera (Heteroptera) in the Ryukyu Islands.

Science Bulletin of Agriculture & Home Economics Division, University of the Ryukyus

4:11–90.

Taniguchi K, Maruyama M, Ichikawa T, Ito F. 2005. A case of Batesian mimicry

between myrmecophilous staphylinid beetle, Pella comes, and its host ant, (Lasius

Dendrolasius) spathepus: an experiment using the Japanese tree frog Hyla japonica as

a real predator. Insectes Sociaux 52(4):320–322 DOI 10.1007/s00040-005-0813-1.

Tomokuni M, Yasunaga T, Takai M, Yamashita I, Kawamura M, Kawasawa T. 1993.

A field guide to Japanese bugs—Terrestrial Heteropterans. Tokyo: Zenkoku Noson

Kyoiku Kyokai(in Japanese).

Walker AA, Mayhew ML, Jin J, Herzig V, Undheim EAB, Sombke A, Fry BG,

Meritt DJ, King GF. 2018. The assassin bug Pristhesancus plagipennis produces

two distinct venoms in separate gland lumens. Nature Communications 9:755

DOI 10.1038/s41467-018-03091-5.

Walker AA, Robinson SD, Undheim EAB, Jin J, Han X, Fry BG, Vetter I, King GF. 2019.

Missiles of mass disruption: composition and glandular origin of venom used as a

projectile defensive weapon by the assassin bug Platymeris rhadamanthus. Toxins

11(11):673 DOI 10.3390/toxins11110673.

Walker AA, Weirauch C, Fry BG, King GF. 2016. Venoms of heteropteran insects: a treasure trove of diverse pharmacological toolkits. Toxins 8(2):43

DOI 10.3390/toxins8020043.

Wattanachaiyingcharoen W, Jongjitvimol T. 2007. First record of the predator,

Pahabengkakia piliceps Miller, 1941 (Reduviidae, Harpactorinae) in the stingless bee,

Trigona collina Smith, 1857 (Apidae, Meliponinae) in Thailand. The Natural History

Journal of Chulalongkorn University 7(1):71–74.

Willemse L. 1985. A taxonomic revision of the New World species of Sirthenea (Heteroptera: Reduviidae: Peiratinae). Zoologische Verhandelingen 215(1):3–67.

Williams BL, Hanifin CT, Brodie Jr ED, Brodie III ED. 2010. Tetrodotoxin affects

survival probability of rough-skinned newts (Taricha granulosa) faced with TTXresistant garter snake predators (Thamnophis sirtalis). Chemoecology 20(4):285–290

DOI 10.1007/s00049-010-0057-z.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

25/26

Winters AE, Wilson NG, Van den Berg CP, How MJ, Endler JA, Marshall NJ, White

AM, Garson MJ, Cheney KL. 2018. Toxicity and taste: unequal chemical defences in a mimicry ring. Proceedings of the Royal Society B 285(1880):20180457

DOI 10.1098/rspb.2018.0457.

Yahiro K, Fujimoto T, Tokuda M, Yano K. 1992. Species composition and seasonal

abundance of ground beetles (Coleoptera) in paddy fields. Japanese Journal of

Entomology 60(4):805–813.

Yasunaga T, Maehara S, Ishikawa T, Takai M. 2018. Guidebook to the heteropteran

world—Basic ecology, morphology, classification and research methodology. Tokyo:

Zenkoku Noson Kyoiku Kyokai(in Japanese).

Zhang G, Weirauch C. 2014. Molecular phylogeny of Harpactorini (Insecta: Reduviidae):

correlation of novel predation strategy with accelerated evolution of predatory leg

morphology. Cladistics 30(4):339–351 DOI 10.1111/cla.12049.

Sugiura and Hayashi (2023), PeerJ, DOI 10.7717/peerj.15380

26/26

...