Advertisement

Synchronized hatching as a possible strategy to avoid sibling cannibalism in stink bugs

Abstract

In some animals, timing of egg hatching is adjusted in response to cues from clutch mates to synchronize hatching within a clutch and this typically facilitates mass migration of hatchlings from their natal clutch. A recent study in eight species of Pentatomidae revealed that four species show synchronized hatching due to responses to earlier-hatched siblings, by comparing temporal hatching patterns between intact clutches and eggs individually detached from clutches. However, hatchlings of Pentatomidae do not migrate from their natal clutch immediately. In the present study, using the same eight species, we explored the evolutionary reason for the synchronized hatching in Pentatomidae. In all of the species examined except one non-synchronized species, Eurydema rugosum, hatchlings showed egg feeding behavior with greatly different time of onset. The highly synchronized species, Halyomorpha halys and Nezara viridula, had the time of onset of egg feeding earlier than in the other species. In these two species, based on the hatching patterns of eggs individually detached from their clutches, we concluded that eggs can be cannibalized by their earlier-hatched siblings unless they hatch in response to siblings. On the other hand, this was not the case in the moderately synchronized species, Piezodorus hybneri and Plautia stali. In the other three non-synchronized species, Aelia fieberi, Dolycoris baccarum, and Palomena angulosa, eggs seemed not to incur a risk of cannibalism. In intact H. halys clutches, almost no eggs were cannibalized by siblings. In conclusion, synchronized hatching serves as a possible strategy to avoid sibling cannibalism in Pentatomidae, although it can also have some other functions.

Significance statement

Eggs should often be able to control when to hatch in response to environmental factors affecting survival of eggs or hatchlings. Species of various taxa show responses to siblings in the same clutch to achieve synchronized hatching among the siblings. It is typically recognized that such synchronized hatching is required so that hatchlings leave their natal clutch together, which serves, for example, to reduce the risk of being preyed on by predators. Here, we present evidence supporting that synchronized hatching observed in some stink bugs helps eggs to avoid being cannibalized by their earlier-hatched siblings. We also show that other stink bugs with no synchronized hatching have no or little risk of sibling egg cannibalism. This study deepens our knowledge that the synchronized hatching can function in various social contexts with siblings.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3

Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Acebes-Doria AL, Leskey TC, Bergh JC (2016a) Development and comparison of trunk traps to monitor movement of Halyomorpha halys nymphs on host trees. Entomol Exp Appl 158:44–53

  2. Acebes-Doria AL, Leskey TC, Bergh JC (2016b) Host plant effects on Halyomorpha halys (Hemiptera: Pentatomidae) nymphal development and survivorship. Environ Entomol 45:663–670

  3. Calizotti GS, Panizzi AR (2014) Behavior of first instar nymphs of Edessa meditabunda (F.) (Hemiptera: Pentatomidae) on the egg mass. Fla Entomol 97:277–280

  4. Colbert PL, Spencer RJ, Janzen FJ (2010) Mechanism and cost of synchronous hatching. Funct Ecol 24:112–121

  5. Collie K, Kim SJ, Baker MB (2013) Fitness consequences of sibling egg cannibalism by neonates of the Colorado potato beetle, Leptinotarsa decemlineata. Anim Behav 85:329–338

  6. 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 176–213

  7. Dickinson JL (1992) Egg cannibalism by larvae and adults of the milkweed leaf beetle (Labidomera clivicollis, Coleoptera: Chrysomelidae). Ecol Entomol 17:209–218

  8. Doody JS, Stewart B, Camacho C, Christian K (2012) Good vibrations? Sibling embryos expedite hatching in a turtle. Anim Behav 83:645–651

  9. Eickwort KR (1973) Cannibalism and kin selection in Labidomera clivicollis (Coleoptera: Chrysomelidae). Am Nat 107:452–453

  10. Elgar MA, Crespi BJ (eds) (1992) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford

  11. Endo J, Numata H (2017) Effects of embryonic responses to clutch mates on egg hatching patterns of Pentatomidae (Heteroptera). Physiol Entomol 42:412–417

  12. Endo J, Takanashi T, Mukai H, Numata H (2019) Egg-cracking vibration as a cue for stink bug siblings to synchronize hatching. Curr Biol 29:143–148

  13. Fréchette B, Coderre D (2000) Oviposition strategy of the green lacewing Chrysoperla rufilabris (Neuroptera: Chrysopidae) in response to extraguild prey availability. Eur J Entomol 97:507–510

  14. Gomi T, Natsuyama M, Sasaki N (2015) Effects of sibling egg cannibalism on the development and survival of Chrysomela populi (Coleoptera: Chrysomelidae). Appl Entomol Zool 50:451–455

  15. Hokyo N, Kiritani K (1962) Sampling design for estimating the population of the southern green stink bug, Nezara viridula (Pentatomidae, Hemiptera) in the paddy field. Jpn J Ecol 12:228–235

  16. Kawada H, Kitamura C (1983) The reproductive behavior of the brown marmorated stink bug, Halyomorpha mista Uhler (Heteroptera: Pentatomidae) I. Observation of mating behavior and multiple copulation. Appl Entomol Zool 18:234–242

  17. Kawai A (1978) Sibling cannibalism in the first instar larvae of Harmonia axyridis Pallas (Coleoptera, Coccinellidae). Kontyû 46:14–19

  18. Kiritani K (1964) The effect of colony size upon the survival of larvae of the southern green stink bug, Nezara viridula. Jpn J Appl Entomol Zool 8:45–53

  19. Kiritani K, Kimura K (1966) A study on the nymphal aggregation of the cabbage stink bug, Eurydema rugosum Motschulsky (Heteroptera: Pentatomidae). Appl Entomol Zool 1:21–28

  20. Kiritani K, Nakasuji F, Hokyo N (1966) The survival rate of eggs and larvae in relation to group size in the southern green stink bug, Nezara viridula L. Jpn J Appl Entomol Zool 10:205–211 [in Japanese with English abstract]

  21. Kirk HM (1988) Cannibalism in a Chrysomelid beetle, Gastrophysa viridula. Dissertation, University of Liverpool

  22. Kutcherov D (2015) Egg-hatching synchrony and larval cannibalism in the dock leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae). Zoology 118:433–438

  23. Lee DH, Nielsen AL, Leskey TC (2014) Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) evaluated under laboratory and field conditions. J Insect Behav 27:639–651

  24. Lockwood JA, Story RN (1985) Photic, thermic, and sibling influences on the hatching rhythm of the southern green stink bug, Nezara viridula (L.). Environ Entomol 14:562–567

  25. Lockwood JA, Story RN (1986) Adaptive functions of nymphal aggregation in the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Environ Entomol 15:739–749

  26. Michaud JP, Grant AK (2004) Adaptive significance of sibling egg cannibalism in Coccinellidae: comparative evidence from three species. Ann Entomol Soc Am 97:710–719

  27. Mock DW, Parker GA (1998) The evolution of sibling rivalry. Oxford University Press, Oxford

  28. Morimoto N (1965) Synchronization of hatching in an egg mass of the cabbage stink bug, Eurydema rugosa. Jpn J Appl Entomol Zool 9:125–126 [in Japanese]

  29. Mukai H, Hironaka M, Tojo S, Nomakuchi S (2012) Maternal vibration induces synchronous hatching in a subsocial burrower bug. Anim Behav 84:1443–1448

  30. Mukai H, Hironaka M, Tojo S, Nomakuchi S (2018) Maternal hatching synchronization in a subsocial burrower bug mitigates the risk of future sibling cannibalism. Ecol Evol 8:3376–3381

  31. Nielsen AL, Hamilton GC, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355

  32. Nishide Y, Tanaka S (2016) Desert locust, Schistocerca gregaria, eggs hatch in synchrony in a mass but not when separated. Behav Ecol Sociobiol 70:1507–1515

  33. O’Connor RJ (1978) Brood reduction in birds: selection for fratricide, infanticide and suicide? Anim Behav 26:79–96

  34. Osawa N (1992) Sibling cannibalism in the ladybird beetle Harmonia axyridis: fitness consequences for mother and offspring. Res Popul Ecol 34:45–55

  35. Perry JC, Roitberg BD (2005) Games among cannibals: competition to cannibalize and parent-offspring conflict lead to increased sibling cannibalism. J Evol Biol 18:1523–1533

  36. Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251

  37. Provine RR (1976) Eclosion and hatching in cockroach first instar larvae: a stereotyped pattern of behaviour. J Insect Physiol 22:127–131

  38. Richardson ML, Mitchell RF, Reagel PF, Hanks LM (2010) Causes and consequences of cannibalism in noncarnivorous insects. Annu Rev Entomol 55:39–53

  39. Root RB, Chaplin SJ (1976) The life-styles of tropical milkweed bugs, Oncopeltus (Hemiptera: Lygaeidae) utilizing the same hosts. Ecology 57:132–140

  40. Spencer RJ, Thompson MB, Banks PB (2001) Hatch or wait? A dilemma in reptilian incubation. Oikos 93:401–406

  41. Stevens L (1992) Cannibalism in beetles. In: Elgar MA, Crespi BJ (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 256–276

  42. Stoleson SH, Beissinger SR (1995) Hatching asynchrony and the onset of incubation in birds, revisited. In: Power DM (ed) Current ornithology, vol 12. Springer, Boston, pp 191–270

  43. Taylor CM (2016) Understanding the relationship between the brown marmorated stink bug, Halyomorpha halys (Stål), and its symbiont, Pantoea carbekii, with implications for stink bug management. Dissertation, University of Maryland

  44. Todd JW (1989) Ecology and behavior of Nezara viridula. Annu Rev Entomol 34:273–292

  45. Warkentin KM (2011) Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integr Comp Biol 51:14–25

  46. Warkentin KM, Caldwell MS (2009) Assessing risk: embryos, information, and escape hatching. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II: the evolutionary ecology of information processing and decision-making. University of Chicago Press, Chicago, pp 177–200

  47. Woolf NK, Bixby JL, Capranica RR (1976) Prenatal experience and avian development: brief auditory stimulation accelerates the hatching of Japanese quail. Science 194:959–960

  48. Yuan ML, Zhang QL, Guo ZL, Wang J, Shen YY (2015) Comparative mitogenomic analysis of the superfamily Pentatomoidea (Insecta: Hemiptera: Heteroptera) and phylogenetic implications. BMC Genomics 16:460

Download references

Acknowledgments

We thank Kazuhiko Kuge and Masaho Haikata for assistance in collecting insects, Elizabeth Nakajima for linguistic corrections, and Yoshito Suzuki and Akira Mori for advice.

Author information

Correspondence to Hideharu Numata.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by J. C Choe

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Endo, J., Numata, H. Synchronized hatching as a possible strategy to avoid sibling cannibalism in stink bugs. Behav Ecol Sociobiol 74, 16 (2020) doi:10.1007/s00265-020-2799-0

Download citation

Keywords

  • Avoidance of cannibalism
  • Halyomorpha halys
  • Nezara viridula
  • Pentatomidae
  • Sibling cannibalism
  • Stink bug
  • Synchronized hatching