Skip to main content
Log in

Disease, contagious cannibalism, and associated population crash in an omnivorous bug, Geocoris pallens

  • Population ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Disease and cannibalism are two strongly density-dependent processes that can suppress predator populations. Here we show that California populations of the omnivorous predatory bug Geocoris pallens are subject to infection by a pathogen, as yet unidentified, that elicits elevated expression of cannibalism. Laboratory experiments showed that the pathogen is moderately virulent, causing flattened abdomens, elevated nymphal mortality, delayed development, and reduced body size of adult females. Infection furthermore increases the expression of cannibalism. Field populations of Geocoris spp. declined strongly in association with sharp increases in the expression of egg cannibalism by adult G. pallens. Increased cannibalism was accompanied by a strongly bimodal distribution of cannibalism expression, with some females (putatively uninfected) expressing little cannibalism and others (putatively infected) consuming most or all of the eggs present. Highly cannibalistic females did not increase their consumption of Ephestia cautella moth eggs, suggesting that the high cannibalism phenotype reflected a specific loss of restraint against eating conspecifics. Highly cannibalistic females also often exhibited reduced egg laying, consistent with a virulent pathogen; less frequently, more cannibalistic females exhibited elevated egg laying, suggesting that cannibalism might also facilitate recycling of nutrients in eggs. Elevated cannibalism was not correlated with reduced prey availability or elevated field densities of G. pallens. Geocoris pallens population crashes appear to reflect the combined consequences of direct virulence—adverse pathogen effects on the infected host’s physiology—and indirect virulence—mortality of both infected and uninfected individuals due to elevated cannibalism expression by infected individuals.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alizon S, Hurford A, Mideo N et al (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol 22:245–259

    Article  CAS  PubMed  Google Scholar 

  • Barabás G, Michalska-Smith MJ, Allesina S (2017) Self-regulation and the stability of large ecological networks. Nat Ecol Evol 1:1870–1875

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B et al (2017) Package ‘lme4’. http://lme4.r-forge.r-project.org/. Accessed 1 Dec 2017

  • Bolker BM, de Castro F, Storfer A et al (2008) Disease as a selective force precluding widespread cannibalism: a case study of an iridovirus of tiger salamanders, Ambystoma tigrinum. Evol Ecol Res 10:105–128

    Google Scholar 

  • Bugg RL, Ehler LE, Wilson LT (1987) Effect of common knotweed (Polygonum aviculare) on abundance and efficiency of insect predators of crop pests. Hilgardia 55(7):1–53

    Article  Google Scholar 

  • Bunke M, Alexander ME, Dick JTA et al (2015) Eaten alive: cannibalism is enhanced by parasites. R Soc Open Sci 2:140369

    Article  PubMed  PubMed Central  Google Scholar 

  • Claessen D, de Roos AM, Persson L (2004) Population dynamic theory of size-dependent cannibalism. Proc R Soc Lond B 271:333–340

    Article  Google Scholar 

  • Crocker RL, Whitcomb WH (1980) Feeding niches of the big-eyed bugs Geocoris bullatus, G. punctipes, and G. uliginosus (Hemiptera: Lygaeidae: Geocorinae). Environ Entomol 9:508–513

    Article  Google Scholar 

  • de Valpine P, Rosenheim JA (2008) Field-scale roles of density, temperature, nitrogen, and predation on aphid population dynamics. Ecology 89:532–541

    Article  PubMed  Google Scholar 

  • Ebert D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Syst 44:623–643

    Article  Google Scholar 

  • Eubanks MD, Denno RF (1999) The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80:1253–1266

    Article  Google Scholar 

  • Hood WR (2012) A test of bone mobilization relative to reproductive demand: skeletal quality is improved in cannibalistic females with large litters. Physiol Biochem Zool 85:385–396

    Article  CAS  PubMed  Google Scholar 

  • Law YH, Rosenheim JA (2011) Effects of combining an intraguild predator with a cannibalistic intermediate predator on a species-level trophic cascade. Ecology 92:333–341

    Article  PubMed  Google Scholar 

  • Law YH, Rosenheim JA (2013) Presence of conspecific females motivates eg cannibalism owing to lower risk of filial cannibalism. Anim Behav 85:403–409

    Article  Google Scholar 

  • Lourdais O, Brischoux F, Shine R, Bonnet X (2005) Adaptive maternal cannibalism in snakes (Epicrates cenchria maurus, Boidae). Biol J Linn Soc 84:767–774

    Article  Google Scholar 

  • Maechler M (2016) Package ‘diptest’. https://CRAN.R-project.org/package=diptest. Accessed 1 Dec 2017

  • Orrock J, Connolly B, Kitchen A (2017) Induced defences in plants reduce herbivory by increasing cannibalism. Nat Ecol Evol 1:1205–1207

    Article  PubMed  Google Scholar 

  • Pereira LS, Keppeler FW, Agostinho AA et al (2017a) Is there a relationship between fish cannibalism and latitude or species richness? PLoS One 12:e0169813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira LS, Agostinho AA, Winemiller KO (2017b) Revisiting cannibalism in fishes. Rev Fish Biol Fisheries 27:499–513

    Article  Google Scholar 

  • Persson L, de Roos AM, Claessen D et al (2003) Gigantic cannibals driving a whole-lake trophic cascade. Proc Nat Acad Sci USA 100:4035–4039

    Article  CAS  PubMed  Google Scholar 

  • Pfennig DW (1997) Kinship and cannibalism. BioScience 47(10):667–675

    Article  Google Scholar 

  • Pfennig DW, Ho SG, Hoffman EA (1998) Pathogen transmission as a selective force against cannibalism. Anim Behav 55(5):1255–1261

    Article  CAS  PubMed  Google Scholar 

  • Pizzatto L, Shine R (2011) You are what ou eat: parasite transfer in cannibalistic cane toads. Herpetologica 67:118–123

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Poulin R, Maure F (2015) Host manipulation by parasites: a look back before moving forward. Trends Parasitol 31(11):563–570

    Article  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 1 Dec 2017

  • Redman EM, Wilson K, Cory JS (2016) Trade-offs and mixed infections in an obligate-killing insect pathogen. J Anim Ecol 85:1200–1209

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ricker WE (1954) Stock and recruitment. J Fish Res Board Canada 11:559–623

    Article  Google Scholar 

  • Ridgway RL, Jones SL (1968) Plant feeding by Geocoris pallens and Nabis americoferus. Annals Entomol Soc Am 61:232–233

    Article  Google Scholar 

  • Rosenheim JA (2005) Intraguild predation of Orius tristicolor by Geocoris spp. and the paradox of irruptive spider mite dynamics in California cotton. Biol Control 32:172–179

    Article  Google Scholar 

  • Rudolf VHW, Antonovics J (2007) Disease transmission by cannibalism: rare event or common occurrence? Proc R Soc Lond B 274:1205–1210

    Article  Google Scholar 

  • Rudolf VHW, Kamo M, Boots M (2010) Cannibals in space: the coevolution of cannibalism and dispersal in spatially structured populations. Am Nat 175(5):513–524

    Article  PubMed  Google Scholar 

  • Sadeh A, Rosenheim JA (2016) Cannibalism amplifies the spread of vertically-transmitted pathogens. Ecology 97:1994–2002

    Article  PubMed  Google Scholar 

  • Sadeh A, Northfield TD, Rosenheim JA (2016) The epidemiology and evolution of parasite transmission through cannibalism. Ecology 97:2003–2011

    Article  PubMed  Google Scholar 

  • Scharf I (2016) The multifaceted effects of starvation on arthropod behaviour. Anim Behav 119:37–48

    Article  Google Scholar 

  • Schausberger P (2003) Cannibalism among phytoseiid mites: a review. Exp Appl Acarol 29:173–191

    Article  PubMed  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, Oxford

    Google Scholar 

  • Takizawa T, Snyder WE (2011) Cannibalism and intraguild predation of eggs within a diverse predator assemblage. Environ Entomol 40:8–14

    Article  PubMed  Google Scholar 

  • Thomas F, Rigaud T, Brodeur J (2012) Evolutionary routes leading to host manipulation by parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 16–33

    Chapter  Google Scholar 

  • Van Allen BG, Dillemuth FP, Flick AJ et al (2017) Cannibalism and infectious disease: friends or foes? Am Nat 190:299–312

    Article  PubMed  Google Scholar 

  • Whitfield JT, Pako WH, Collinge J et al (2017) Cultural factors that affected the spatial and temporal epidemiology of kuru. R Soc Open Sci 4:160789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise DH (2006) Cannibalism, food limitation, intraspecific competition, and the regulation of spider populations. Annu Rev Entomol 51:441–465

    Article  CAS  PubMed  Google Scholar 

  • Yan G, Stevens L, Schall JJ (1994) Behavioral changes in Tribolium beetles infected with a tapeworm: variation in effects between beetle species and among genetic strains. Am Nat 143:830–847

    Article  Google Scholar 

Download references

Acknowledgements

We thank Nick Groenenberg, Joe Baird, and the late Steve Orloff who provided help over many years in locating suitable fields for our sampling; Benjamin Maples and Shucun Sun for assistance in the field and helpful discussions; Norma Ordaz and Anthony Le for invaluable help with the infection experiments; Maria T. Gonzalez for assistance with primer design, virus purification, RNA/DNA libraries, and sequencing; Tobin Northfield for helping to reconstruct the record of informal sampling efforts; and Ian Grettenberger for locating old data sets. This work was supported by funding from USDA AFRI Grant no. 2009-02096, Postdoctoral Award no. FI-457-2011 from BARD (The United States-Israel Binational Agricultural Research and Development Fund), and BSF (US-Israel Binational Science Foundation) Grant 2013-306. We dedicate this paper to the memory of our colleague Larry Godfrey, who passed away during the preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

JAR, AS, NB, MCM, TM, RK, WBH, and YHL conceived the idea for the study and designed the work; all authors collected the data; JAR and AS analyzed the data and led the writing with input from all authors.

Corresponding authors

Correspondence to Jay A. Rosenheim or Asaf Sadeh.

Additional information

Communicated by Evan Siemann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 111 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosenheim, J.A., Booster, N.A., Culshaw-Maurer, M. et al. Disease, contagious cannibalism, and associated population crash in an omnivorous bug, Geocoris pallens. Oecologia 190, 69–83 (2019). https://doi.org/10.1007/s00442-019-04407-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04407-y

Keywords

Navigation