, Volume 96, Issue 2, pp 201–211 | Cite as

Pre- and post-hatch trophic egg production in the subsocial burrower bug, Canthophorus niveimarginatus (Heteroptera: Cydnidae)

  • Lisa FilippiEmail author
  • Narumi Baba
  • Koichi Inadomi
  • Takao Yanagi
  • Mantaro Hironaka
  • Shintaro Nomakuchi
Original Paper


In recent years, three terrestrial bugs, Adomerus triguttulus and Sehirus cinctus (Cydnidae) and the closely related Parastrachia japonensis (Parastrachiidae), have been the focus of several fascinating studies because of the remarkable, extensive parental care they were found to display. This care includes egg and nymph guarding, production of trophic eggs, unfertilized, low cost eggs that are used as food by newly hatched nymphs, and progressive provisioning of the host seed. In this study, we have investigated yet a third related Asian cydnid, Canthophorus niveimarginatus, with regard to the possible occurrence of some or all of these complex traits in order to assess how widespread these maternal investment patterns are in this group of insects and to better understand the implications of their manifestations from an evolutionary context. Manipulative experiments were carried out in the lab to determine whether females provision nests. Observational and egg removal studies were carried out to determine whether trophic eggs are produced, and, if they are, their possible impact on nymphal success. The findings revealed that C. niveimarginatus does, in fact, progressively provision young, and this species also displays all of the other behaviors associated with extended parental care in subsocial insects. Moreover, unlike the other two related species, which place trophic eggs on the surface of the original egg mass, C. niveimarginatus produces both pre- and post-hatch trophic eggs. Nymphs deprived of access to post-hatch trophic eggs had significantly lower body weight and survival rate than those that fed on them. To our knowledge, this is the first time the production of both pre- and post-hatch trophic eggs has been demonstrated in insects outside the Hymenoptera. In this paper, we qualitatively and quantitatively demonstrate the provisioning behavior and patterns of trophic egg production in C. niveimarginatus. When and how trophic eggs are produced and delivered to young should have important correlations with the ecological and life history constraints under which a species has evolved. Thus, we also discuss the possible ecological and life history factors that favor the evolution of post-hatch trophic eggs.


Maternal investment Oophagy Parental care Parent–offspring conflict Progressive provisioning Subsocial Trophic eggs 



We thank Prof. Emeritus S. Tojo (Department of Applied Biological Sciences, Faculty of Agriculture, Saga University) for many useful comments and valuable suggestions. We also thank Y. Goto (Omura City, Nagasaki Prefecture) for valuable advice. This study was funded in part by a grant from The Japan Ministry of Education, Science and Culture, No. 18570025. The experiments carried out in this study comply with the current laws of Japan where they were performed.


  1. Abe Y, Mishiro K, Takanashi M (1995) Symbiont of brown-winged green bug. Plautia stali Scott. Jap J Appl Entomol Zool 39:109–115Google Scholar
  2. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  3. Bains S (1956) The role of the symbiotic bacteria in the nutrition of Rhodnius prolixus (Hemiptera). J Exp Biol 33:533–541Google Scholar
  4. Baur B (1992) Cannibalism in gastropods. In: Elgar MA, Crespi BJ (eds) Cannibalism, ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 102–127Google Scholar
  5. Bell WJ, Bohm MK (1975) Oosorption in insects. Biol Rev 50:373–396PubMedCrossRefGoogle Scholar
  6. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Wiley, NYGoogle Scholar
  7. Crespi BJ (1992) Cannibalism and trophic eggs in subsocial and eusocial insects. In: Elgar MA, Crespi BJ (eds) Cannibalism, ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 176–213Google Scholar
  8. Filippi-Tsukamoto L, Nomakuchi S, Kuki K, Tojo S (1995) Adaptiveness of parental care in Parastrachia japonensis (Hemiptera: Cydnidae). Ann Entomol Soc Am 88:374–383Google Scholar
  9. Filippi L, Hironaka M, Nomakuchi S (2001) A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource. Popul Ecol 43:41–50CrossRefGoogle Scholar
  10. Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacteria of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68:389–396PubMedCrossRefGoogle Scholar
  11. Gobin B, Ito F (2000) Queens and major workers of Acanthomyrmex ferox redistribute nutrients with trophic eggs. Naturwissenschaften 87:323–326PubMedCrossRefGoogle Scholar
  12. Gobin B, Peeters C, Billen J (1998) Production of trophic eggs by virgin workers in the ponerine ant Gnamptogenys menadensis. Physiol Entomol 23:329–336CrossRefGoogle Scholar
  13. Gundermann JL, Horel A, Roland C (1991) Mother–offspring food transfer in Caelotes terrestris (Araneae, Agelenidae). J Arachnol 19:97–101Google Scholar
  14. Gyotoku N, Tachikawa S (1980) Life history of Parastrachia japonensis (Scott) Cydnidae: Sehirinae (in Japanese). Rostria 33:359–368Google Scholar
  15. Heying HE (2001) Social and reproductive behaviour in the Madagascan poison frog, Mantella laevigata, with comparisons to the dendrobatids. Anim Behav 61:567–577CrossRefGoogle Scholar
  16. Hironaka M, Nomakuchi S, Iwakuma S, Filippi L (2005) Trophic egg production in a subsocial shield bug, Parastrachia japonensis Scott (Heteroptera: Parastrachiidae), and its functional value. Ethology 111:1089–1102CrossRefGoogle Scholar
  17. Kim KW, Horel A (1998) Matriphagy in the spider Amaurobius ferox (Araneidae, Amaurobiidae): an example of mother–offspring interactions. Ethology 104:1021–1037CrossRefGoogle Scholar
  18. Kim KW, Roland C (2000) Trophic egg laying in the spider, Amaurobius ferox: mother–offspring interactions and functional value. Behav Processes 50:31–42PubMedCrossRefGoogle Scholar
  19. Kobayashi T (1964) Developmental stages of Geotomus pygmaeus (DALLAS) and Sehirus niveimarginatus (SCOTT) (Cydnidae). Kontyu 32:21–27Google Scholar
  20. Kotaki T (2003) Oosorption in the stink bug, Plautia crossota stali: induction and vitellogenin dynamics. J Insect Phys 49:105–113CrossRefGoogle Scholar
  21. Kudo S, Nakahira T (2004) Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug. Oikos 107:28–34CrossRefGoogle Scholar
  22. Kudo S, Nakahira T (2005) Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions. Oikos 111:459–464CrossRefGoogle Scholar
  23. Kukuk PF (1992) Oophagy as cannibalism in social bees. In: Elgar MA, Crespi BJ (eds) Cannibalism, ecological and evolutionary implications. Oxford University Press, Oxford, pp 214–237Google Scholar
  24. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, OxfordGoogle Scholar
  25. Nakahira T (1994) Production of trophic eggs in the subsocial burrower bug Admerus (sic) triguttulus. Naturwissenschaften 81:413–414Google Scholar
  26. Peeters C (1997) Morphologically primitive ants: Comparative review of social characters, and the importance of queen-worker dimorphism. In: Choe J, Crespi B (eds) Evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge, pp 372–391Google Scholar
  27. Perry JC, Roitberg BD (2005) Ladybird mothers mitigate offspring starvation risk by laying trophic eggs. Behav Ecol Sociobiol 58:578–586CrossRefGoogle Scholar
  28. Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714CrossRefGoogle Scholar
  29. Pie MR (2002) Behavioral repertoire, age polyethism and adult transport in Ectatomma opaciventre (Formicidae: Ponerinae). J Insect Behav 15:25–35CrossRefGoogle Scholar
  30. Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
  31. Polis GA (1984) Intraspecific predation and ‘infant killing’ among invertebrates. In: Hausfater G, Blaffer Hrdy S (eds) Infanticide. Comparative and evolutionary perspectives. Aldine, Hawthorne, NY, pp 87–104Google Scholar
  32. Prado SS, Rubinoff D, Almeida RPP (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99:577–585CrossRefGoogle Scholar
  33. Rosenkranz W (1939) Die Symbiose der Pentatomiden (Hemiptera, Heteroptera). Z Morphol Okol Tiere 36:279–309CrossRefGoogle Scholar
  34. Sites RW, McPherson JE (1982) Life history and laboratory rearing of Sehirus cinctus cinctus (Hemiptera: Cydnidae), with descriptions of immature stages. Ann Entomol Soc Am 75:210–215Google Scholar
  35. Tachikawa S (1991) Studies on subsocialities of Heteroptera in Japan (in Japanese). Tokyo Agricultural University Press, TokyoGoogle Scholar
  36. Tallamy DW, Wood TK (1986) Convergence patterns in subsocial insects. Annu Rev Entomol 31:369–390CrossRefGoogle Scholar
  37. Trivers R (1985) Social evolution. Benjamin Cummings Publishing, San FranciscoGoogle Scholar
  38. Tsukamoto L, Tojo S (1992) A report of progressive provisioning in a stink bug, Parastrachia japonensis (Hemiptera: Cydnidae). J Ethol 10:21–29CrossRefGoogle Scholar
  39. Wardlaw C, Elmes GW (1995) Trophic eggs laid by fertile Myrmica queens (Hymenoptera: Formicidae). Insectes Soc 42:303–308CrossRefGoogle Scholar
  40. West MJ, Alexander RD (1963) Sub-social behaviour in a burrowing cricket Anurogryllus muticus (De Geer), Orthoptera: Gryllidae. Ohio J Sci 63:19–24Google Scholar
  41. Wilson EO (1975) Enemy specification in the alarm-recruitment system of an ant. Science 190:798–800PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Lisa Filippi
    • 1
    Email author
  • Narumi Baba
    • 2
  • Koichi Inadomi
    • 3
  • Takao Yanagi
    • 3
  • Mantaro Hironaka
    • 4
  • Shintaro Nomakuchi
    • 3
  1. 1.Department of BiologyHofstra UniversityHempsteadUSA
  2. 2.Graduate School of Bioresource and Bioenvironmental SciencesKyushu UniversityFukuokaJapan
  3. 3.Department of Applied Biological Sciences, Faculty of AgricultureSaga UniversitySagaJapan
  4. 4.Department of Biology, Faculty of MedicineHamamatsu University School of MedicineHamamatsuJapan

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