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Eggs in faeces: defensive mechanisms and effects of faecal coating by a water scavenger beetle, Coelostoma stultum (Coleopterea: Hydrophilidae)

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Abstract

The egg stage in insect development is vulnerable to fluctuations in environmental conditions and attacks by natural enemies. Protective devices are effective means of avoiding both abiotic and biotic damage to eggs. Although some insects use their faeces as a protective device, few studies have focused on using faeces for egg protection, and studies that examined the mechanism are lacking. Females of a water scavenger beetle, Coelostoma stultum, typically lay eggs and coat them with cocoons and their faeces. The efficacy of a double defensive device, however, remains uncertain. Here, we conducted field observations and laboratory experiments to assess the protective effects of cocoons with faecal coating on eggs against predation and determine the duration and mechanisms of this defence. Our findings reveal that the faeces on the egg cocoon protected eggs from predation by the pill bugs, Armadillidium vulgare, and marsh slugs, Deroceras laeve. Laboratory experiments showed that the defensive effect of faecal coating was maintained for three days and decreased daily. The double protective traits with faecal coating on the egg cocoons protected the eggs from instense predation pressure in C. stultum. The behavioural patterns of the pill bugs and egg predation rates indicate that the faecal coating behaviour in C. stultum protects eggs with chemical compounds and textural camouflage in mud when the antennae of the pill bugs touch faeces. It is important to note that for this defence to be effective, the chemistry and texture of the faeces should be similar to that of the oviposition sites.

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Data availability

The data supporting the findings of this study are available from the corresponding author on reasonable request.

References

  • Birchard GF (1991) Water vapor and oxigen exchange of praying mantis (Tenodera aridifolia sinensis) egg cases. Physiol Zool 64:960–972

    Article  Google Scholar 

  • Borg-Karlson AK, Nordlander G, Mudalige A, Nordenhem H, Unelius CR (2006) Antifeedants in the feces of the pine weevil Hylobius abietis: Identification and biological activity. J Chem Ecol 32:943–957

    Article  CAS  PubMed  Google Scholar 

  • Brown CG, Funk DJ (2005) Aspects of the natural history of Neochlamisus (Coleoptera: Chryomelidae): faecal case-associated life history and behavior, with a method for studying insect constructions. Ann Entomol Soc Am 98:711–725

    Article  Google Scholar 

  • Brown CG, Funk DJ (2010) Antipredatory properties of an animal architecture: how complex faecal cases thwart arthropod attack. Anim Behav 79:127–136

    Article  Google Scholar 

  • CABI (2021) Dashsheet, Deroceras laeve (meadow slug); Invasive Species Compendium. CABI, Wallingford, United Kingdom. http://www.cabi.org/isc/datasheet/85751. Accessed 15 Jan 2021

  • Chaboo CS, Grobbelaar E, Larsen A (2007) Fecal ecology in leaf beetles: novel records in the African arrow-poison beetles, Diamphidia Gerstaecker and Polyclada Chevrolat (Chrysomelidae: Galerucinae). Coleopt Bull 61:297–309

    Article  Google Scholar 

  • Chen SH, Young B (1941) On the protective value of the egg-pedicel of Chrysopidae. Sinensia 12:211–215

    Google Scholar 

  • Damman H, Cappuccino N (1991) Two forms of egg defense in a chrysomelid beetle: egg clumping and excrement cover. Ecol Entomol 16:163–167

    Article  Google Scholar 

  • Eisner T, van Tassell E, Carrel JE (1967) Defensive use of a “fecal shield” by a beetle larva. Science 158:1471–1473

    Article  CAS  PubMed  Google Scholar 

  • Gómez NE, Witte L, Hartmann T (1999) Chemical defense in larval tortoise beetles: essential oil composition of fecal shields of Eurypedus nigrosignata and foliafe of its host plant, Cordia curassavica. J Chem Ecol 25:1007–1027

    Article  Google Scholar 

  • Grossmueller DW, Lederhouse RC (1985) Oviposition site selection: an aid to rapid growth and development in the tiger swallowtail butterfly, Papilio glaucus. Oecologia 66:68–73

    Article  PubMed  Google Scholar 

  • Gullan PJ, Cranston PS (2010) The insects: an outline of entomology, 4th edn. Wiley-Blackwell, USA

    Google Scholar 

  • Hammond RB (1996) Conservation tillage and slugs in the U.S. corn belt. In: Henderson FI (ed) Slug & snail pests in agriculture. British Crop Protection Council, Great Britain, pp 31–38

    Google Scholar 

  • Hansen M (1999) World catalogue of insects. Volume 2. Hydrophiloidea (s. str.) (Coleoptera). Apollo Books, Stenstrup

  • Hayashi M, Nomura H (2014) Eggs of Mallada desjardinsi (Neuroptera: Chrysopidae) are protected by ants: the role of egg stalks in ant-tended aphid colonies. Behavior 43:1003–1007

    Google Scholar 

  • Higashiura Y (1989) Survival of eggs in the gypsy moth Lymantria dispar. II. Oviposition site selection in changing environments. J Anim Ecol 58:413–426

    Article  Google Scholar 

  • Hilker M (1992) Protective devices of early developmental stages in Pyrrhalta viburni (Coleoptera, Chrysomelidae). Oecologia 92:71–75

    Article  PubMed  Google Scholar 

  • Hilker M (1994) Egg deposition and protection of eggs in Chrysomelidae. In: Jolivet PHA, Cox ML, Petitpierre E (eds) Novel aspects of biology of Chrysomelidae. series entomologica 50. Kluwer Academic Publishers, Dordrecht, pp 263–276

    Chapter  Google Scholar 

  • Hinton HE (1981) Biology of insect eggs. Pergamon Press, Oxford

    Google Scholar 

  • Iwata KS, Watanabe M (1957) Alternate turning response in Armadillidium vulgare (5) Sense organ functioning in the response. Zool Mag 66:468–471 (In Japanese with English summary)

    Google Scholar 

  • Jia F, Angus RB, Bian D (2019) Two new species of Coelostoma Brullé, 1835 from China (Coleoptera: Hydrophilidae: Sphaeridiinae). Aquat Insects 40:291–299

    Article  Google Scholar 

  • Kurozumi T (2000) Conservation biology of shellfish in Japan –From the shell mound period to the future. Kaiyo Monthly Extra 20:42–56 (In Japanese)

    Google Scholar 

  • Lancaster J, Downes BJ (2013) Aquatic Entomology. Oxford University Press, United Kingdom

    Book  Google Scholar 

  • Liu HC, Hu FS, Fikáček M (2020) Review of the genus Coelostoma of Taiwan with description of a new species (Coleoptera: Hydrophilidae). Acta Entomol Mus Natl Pragae 60:155–162

    Google Scholar 

  • Machado G, Oliveira PS (2002) Maternal care in the neotropical harvestman Bourguyia albiornata (Arachnida: Opiliones): oviposition site selection and egg protection. Behaviour 139:1509–1524

    Article  Google Scholar 

  • Matsushima R (2019) Fecal coating behavior by Coelostoma stultum (Coleoptera, Hydrophilidae). [translated from Japanese] Sayabane N S 33:45–46 (In Japanese)

    Google Scholar 

  • Matsushima R, Haga T (2021) Predation on the egg of Coelostoma stultum (Coleoptera: Hydrophilidae) by the alien species Deroceras laeve (Mollusca: Gastropoda: Agriolomacidae). Molluscan Res 41:254–261

    Article  Google Scholar 

  • Messina FJ, Root RB (1980) Association between leaf beetles and meadow goldenrods (Solidago spp.) in central New York. Ann Entomol Soc Am 73:641–646

    Article  Google Scholar 

  • Minoshima YN, Seidel M, Wood JR, Leschen RAB, Gunter NL, Fikáček M (2018) Morphology and biology of the flower-visiting water scavenger beetle genus Rygmodus (Coleoptera: Hydrophilidae). Entomol Sci 21:363–384

    Article  Google Scholar 

  • Morton TC, Vencl FV (1998) Larval beetles form a defense from recycled host-plant chemicals discharged as fecal wastes. J Chem Ecol 24:765–785

    Article  CAS  Google Scholar 

  • Müller C, Hilker M (1999) Unexpected reactions of a generalist predator towards defensive devices of cassidine larvae (Coleoptera, Chrysomelidae). Oecologia 118:166–172

    Article  PubMed  Google Scholar 

  • Nafus DM, Schreiner IH (1988) Parental care in a tropical nymphalid butterfly Hypolimnas anomala. Anim Behav 36:1425–1431

    Article  Google Scholar 

  • Nogueira-de-Sá F, Trigo JR (2005) Faecal shield of the tortoise beetle Plagiometriona aff. flavescens (Chrysomelidae: Cassidinae) as chemically mediated defence against predators. J Trop Ecol 21:189–194

    Article  Google Scholar 

  • Nunomura N (1990) Studies on the terrestrial isopod crustaceans in Japan V. Taxonomy of the family Armadillidiidae, Armadiliidae and Tylidae, with Taxonomic supplements to some other families. Bull Toyama Sci Museum 13:1–58 (In Japanese)

    Google Scholar 

  • Ohba S, Maeda A (2017) Parental care behaviour of the giant water bug Kirkaldyia deyrolli (Heteroptera: Belostomatidae) against ants. Ecol Entomol 42:402–410

    Article  Google Scholar 

  • Olmstead KL (1994) Waste products as chrysomelid defenses. In: Jolivet PHA, Cox ML, Petitpierre E (eds) Novel aspects of biology of Chrysomelidae. series entomologica 50. Kluwer Academic Publishers, Dordrecht, pp 311–318

    Chapter  Google Scholar 

  • Olmstead KL, Denno RF (1992) Cost of shield defence for tortoise beetles (Coleoptera: Chrysomelidae). Ecol Entomol 17:237–243

    Article  Google Scholar 

  • Olmstead KL, Denno RF (1993) Effectiveness of tortoise beetle larval shields against different predator species. Ecology 74:1394–1405

    Article  Google Scholar 

  • Peterson A (1963) Egg types among moths of the Pyralidae and Phycitidae-Lepidoptera. Fla Entomol 46:1–14

    Article  Google Scholar 

  • R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org. Accessed 4 Feb 2021

  • Růžička Z (1997) Protective role of the egg stalk in Chrysopidae. Eur J Entomol 94:111–114

    Google Scholar 

  • Santos ESA, Bueno PP, Gilbert JDJ, Machado G (2017) Macroecology of parental care in arthropods: higher mortality risk leads to higher benefits of offspring protection in tropical climates. Biol Rev 92:1688–1701

    Article  PubMed  Google Scholar 

  • Schmalfuss H (2003) World catalog of terrestrial isopods (Isopoda: Oniscidea). Stuttg Beitr zur Naturkd Serie A (Biologie) 654:1–341

    Google Scholar 

  • Schmitz EH (1986) Cephalothoracic muscles of the foregut and feeding appendages of Armadillidium vulgare (Latreille) (Crustacea: Isopoda). J Crustac Biol 6:134–142

    Article  Google Scholar 

  • Schulte VF (1988) Zum kokonbau- und eiablage-verhalten dungbewohnender Cercyon-Arten (Coleoptera: Hydrophilidae). Entomol Blätter 84:95–103

    Google Scholar 

  • Sherman M, Tamashiro M (1954) The sweetpotato weevils in Hawaii: their biology and control. Tech Bull Hawaii Agric Exp Stn Univ Hawaii 23:1–36

    Google Scholar 

  • Slater PJB (1981) Individual differences in animal behaviour. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology. Plenum Press, NewYork, pp 35–49

    Chapter  Google Scholar 

  • South A (1992) Terrestrial slugs. Biology, ecology and control. Chapman & Hall, London

    Book  Google Scholar 

  • Spedicato G (2017) Discrete time markov chains with R. R J 09:84–104

    Article  Google Scholar 

  • Stewart PD, Macdonald DW, Newman C, Cheeseman CL (2001) Boundary faeces and matched advertisement in the European badger (Meles meles): a potential role in range exclusion. J Zool 255:191–198

    Article  Google Scholar 

  • Tallamy DW, Wood TK (1986) Convergence patterns in subsocial insects. Ann Rev Entomol 31:369–390

    Article  Google Scholar 

  • Vencl FV, Morton TC, Mumma RO, Schultz JC (1999) Shield defense of a larval tortoise beetle. J Chem Ecol 25:549–566

    Article  CAS  Google Scholar 

  • Wiktor A (2000) Agriolimacidae (Gastropoda: Pulmonata) — a systematic monograph. Ann Zool 49:347–590

    Google Scholar 

  • Wiktor A, Auffenburg K (2002) Contribution to the knowledge of the terrestrial slugs of Pakistan. Folia Malacol 10:9–15

    Article  Google Scholar 

  • Williams EH (1981) Thermal influences on oviposition in the montane butterfly Euphydryas gillettii. Oecologia 50:342–346

    Article  PubMed  Google Scholar 

  • Woodman JD (2017) Effects of substrate salinity on oviposition, embryonic development and survival in the Australian plague locust, Chortoicetes terminifera (Walker). J Insect Physiol 96:9–13

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We appreciate Dr Martin Fikáček (National Sun Yat-sen University, Taiwan) and Dr Yûsuke N. Minoshima (Kitakyushu Museum of Natural History and Human History) for their insightful comments and for providing some important information related to Hydrophilidae. We want to thank Toshiko Sakai for her willingness to permit us to conduct experiments at the study site. We are also deeply grateful to Dr Mitsuru Hirota (University of Tsukuba) and Dr Yukie Sato (University of Tsukuba) for their crucial comments and constructive suggestions regarding the manuscript. We thank Dr Kazumu Kuramitsu (University of Tsukuba) and members of the Conservation Ecology Laboratory of University of Tsukuba for their valuable comments.

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All authors contributed to the study conception and design. Project design: Ryosuke Matsushima and Tomoyuki Yokoi. Data collection and analysis: Ryosuke Matsushima. Manuscript writing: Ryosuke Matsushima and Tomoyuki Yokoi. The authors read and approved the final manuscript.

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Correspondence to Ryosuke Matsushima or Tomoyuki Yokoi.

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Communicated by: Matthias Waltert

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114_2023_1857_MOESM1_ESM.xlsx

Supplementary file1 (XLSX 39 KB) Table S1 Transition matrices of observed behaviour in eight individuals of the pill bug, Armadillidium vulgare, for each treatment. These matrices indicate each behaviour (columns) and followed each behaviour (rows). (A) control, (B) no-coating, (C) artificial coating, (D) mud coating

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Matsushima, R., Yokoi, T. Eggs in faeces: defensive mechanisms and effects of faecal coating by a water scavenger beetle, Coelostoma stultum (Coleopterea: Hydrophilidae). Sci Nat 110, 29 (2023). https://doi.org/10.1007/s00114-023-01857-6

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