Skip to main content
Log in

Filial cannibalism in spottail darters (Etheostoma squamiceps) includes the targeted removal of infected eggs

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The ubiquity of freshwater molds makes them important sources of disease in aquatic organisms and their eggs and has selected for defense mechanisms in fishes and amphibians. Previous studies have shown that, among fishes, the presence of nest-guarding males can reduce egg losses due to infection; however, how much infection males encounter and whether they actively target infected eggs or consume them during cannibalism for other reasons has not been investigated. In a 2-year laboratory study, I artificially raised broods of spottail darter (Etheostoma squamiceps) eggs to determine whether the potential rate of egg loss to Saprolegnia infection was significant enough to select for the targeting of infected eggs. Broods were inspected daily and infected eggs were removed; infections occurred across the broods and throughout the 11–13 days of development. Egg loss due to infection was significant and varied between years, with concomitant reductions in fry production. In a separate laboratory study, I found that 10 male spottail darters consumed both healthy and Saprolegnia-infected eggs, but half of the males consumed infected eggs at rates significantly greater than expected by chance. The results show that Saprolegnia infection is significant and temporally variable, and that guarding males can respond by non-randomly consuming infected eggs.

Significance statement

In many species of fishes in which males guard their eggs, they also eat some of those eggs (filial cannibalism). One possible explanation for this behavior in freshwater fishes is that males are consuming eggs that have become infected with water mold, reducing its spread to other eggs. This hypothesis predicts that (1) egg loss due to infection is potentially significant if not controlled and (2) egg-guarding males can detect and target infected eggs for consumption. I confirmed both of these predictions in laboratory experiments using the spottail darter, a freshwater fish found in midwestern North America. This result supports an adaptive explanation for filial cannibalism, a seemingly nonadaptive behavior.

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

Similar content being viewed by others

References

  • Bandoli JH (1997) Factors influencing reproductive success in male spottail darter (Etheostoma squamiceps, Pisces, Percidae). Proc Indiana Acad Sci 106:145–157

    Google Scholar 

  • Bandoli JH (2002) Brood defense and filial cannibalism in the spottail darter (Etheostoma squamiceps): the effects of parental status and prior experience. Behav Ecol Sociobiol 51:222–226

    Article  Google Scholar 

  • Bandoli JH (2006) Male spottail darters (Etheostoma squamiceps) do not use chemical or positional cues to discriminate between sired and foster eggs. Behav Ecol Sociobiol 59:606–613

    Article  Google Scholar 

  • Blaustein AR, Hokit DG, O’Hara RK, Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the Pacific Northwest. Biol Conserv 67:251–254

    Article  Google Scholar 

  • Bruno DW, Van West P, Beakes GW (2011) Saprolegnia and other oomycetes. In: Woo P, Bruno D (eds) Fish Diseases and disorders, vol 3. CAB International, pp 669–720

  • Dix NJ, Webster J (1995) Fungal ecology. Chapman and Hall, London

    Book  Google Scholar 

  • Elgar M, Crespi B (eds) (1992) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford

    Google Scholar 

  • Emlen A, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Benéitez MJ, Ortiz-Santaliestra ME, Lizana M, Diéguez-Uribeondo J (2011) Differences in susceptibility to Saprolegnia infections among embryonic stages of two anuran species. Oecologia 165:819–826

    Article  PubMed  Google Scholar 

  • Gomagano D, Kohda M (2008) Partial filial cannibalism enhances initial body condition and size in parental car fish with strong male-male competition. Ann Zool Fenn 45:55–65

    Article  Google Scholar 

  • Gomez-Mestre I, Touchon JC, Warkentin KM (2006) Amphibian embryo and parental defenses and a larval predator reduce egg mortality from water mold. Ecology 87:2570–2581

    Article  PubMed  Google Scholar 

  • Gray SM, Dill LM, McKinnon JS (2007) Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases. Am Nat 169:258–263

    Article  PubMed  Google Scholar 

  • Hughes GC (1994) Saprolegniasis, then and now: a retrospective. In: Mueller G (ed) Salmon saprolegniasis. Dept. of Energy, Bonneville Power Administration, Portland, Oregon, pp 3–32

    Google Scholar 

  • Hussein MMA, Hatai K, Nomura T (2001) Saprolegniosis in salmonids and their eggs in Japan. J Wildlife Dis 37:204–207

    Article  CAS  Google Scholar 

  • Klug H, Bonsall MB (2007) When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. Am Nat 170:886–901

    Article  PubMed  Google Scholar 

  • Klug H, Chin A, St Mary CM (2005) The net effects of guarding on egg survivorship in the flagfish, Jordanella floridae. Anim Behav 69:661–668

    Article  Google Scholar 

  • Klug H, Lindström K, St. Mary C (2006) Parents benefit from eating offspring: density-dependent egg survivorship compensates for filial cannibalism. Evolution 60:2087–2095

    Article  PubMed  Google Scholar 

  • Knouft JH, Page LM, Plewa MJ (2003) Antimicrobial egg cleaning by the fringed darter (Perciformes: Percidae: Etheostoma crossopterum): implications of a novel component of parental care in fishes. Proc R Soc Lond B 270:2405–2411

    Article  Google Scholar 

  • Kraak SBM (1996) Female preference and filial cannibalism in Aidablennius sphynx (Teleostei, Blenniidae); a combined field and laboratory study. Behav Process 36:85–98

    Article  CAS  Google Scholar 

  • Lake CT (1936) The life history of the fan-tailed darter. Am Midl Nat 17:816–830

    Article  Google Scholar 

  • Lehtonen TK, Kvarnemo C (2015a) Infections may select for filial cannibalism by impacting egg survival in interactions with water salinity and egg density. Oecologia 178:673–683

    Article  PubMed  Google Scholar 

  • Lehtonen TK, Kvarnemo C (2015b) Density effects on fish egg survival and infections depend on salinity. Mar Ecol-Prog Ser 540:183–191

    Article  Google Scholar 

  • Lindström K, Hellström M (1993) Male size and parental care in the sand goby, Pomatoschistus minutus. Ethol Ecol Evol 5:97–106

    Article  Google Scholar 

  • Lindström K, Sargent RC (1997) Food access, brood size and filial cannibalism in the fantail darter, Etheostoma flabellare. Behav Ecol Sociobiol 40:107–110

    Article  Google Scholar 

  • Lissåker M, Kvarnemo C, Svensson O (2003) Effects of a low oxygen environment on the parental effort and filial cannibalism in the male sand goby, Pomatoschistus minutus. Behav Ecol 14:374–381

    Article  Google Scholar 

  • Magnhagen C (1986) Activity differences influencing food selection in the marine fish Pomatoschistus microps. Can J Fish Aquat Sci 43:223–227

    Article  Google Scholar 

  • Manica A (2002a) Filial cannibalism in teleost fish. Biol Rev 77:261–277

    Article  PubMed  Google Scholar 

  • Manica A (2002b) Alternative strategies for a father with a small brood: mate, cannibalise or care. Behav Ecol Sociobiol 51:319–323

    Article  Google Scholar 

  • Mehlis M, Bakker TCM, Engqvist L, Frommen JG (2010) To eat or not to eat: egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism. Proc R Soc Lond B 277:2627–2635

    Article  Google Scholar 

  • Neff BD (2003) Paternity and condition affect cannibalistic behavior in nest-tending bluegill sunfish. Behav Ecol Sociobiol 54:377–384

    Article  Google Scholar 

  • Oláh J, Farkas J (1978) Effect of temperature, pH, antibiotics, formalin and malachite green on the growth and survival of Saprolegnia and Achlya parasitic on fish. Aquaculture 13:273–288

    Article  Google Scholar 

  • Page LM (1974) The life history of the spottail darter, Etheostoma squamiceps, in Big Creek, Illinois and Ferguson Creek, Kentucky. Ill Nat Hist Surv Bull 33:275–295

    Google Scholar 

  • Page LM, Ceas PA, Swofford DL, Buth DG (1992) Evolutionary relationships within the Etheostoma squamiceps complex (Percidae; subgenus Catonotus) with descriptions of five new species. Copeia 1992:615–646

    Article  Google Scholar 

  • Payne AG, Smith C, Campbell AC (2002) Filial cannibalism improves survival and development of beaugregory damselfish embryos. Proc R Soc Lond B 269:2095–2102

    Article  Google Scholar 

  • Payne AG, Smith C, Campbell AC (2004) A model of oxygen-mediated filial cannibalism in fishes. Ecol Model 174:253–266

    Article  Google Scholar 

  • Porterfield JC, Page LM, Near TJ (1999) Phylogenetic relationships among fantail darters (Percidae: Etheostoma: Catonotus): total evidence analysis of morphological and molecular data. Copeia 1999:551–564

    Article  Google Scholar 

  • Rand TG, Munden D (1993) Chemotaxis of zoospores of two fish-egg-pathogenic strains of Saprolegnia diclina (Oomycotina: Saprolegniaceae) toward salmonid egg chorion extracts and selected amino acids and sugars. J Aquat Anim Health 5:240–245

    Article  Google Scholar 

  • Rohwer S (1978) Parent cannibalism of offspring and egg raiding as a courtship strategy. Am Nat 112:429–440

    Article  Google Scholar 

  • Sargent RC (1992) Ecology of filial cannibalism in fish: theoretical perspectives. In: Elgar M, Crespi B (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 38–62

    Google Scholar 

  • Silphaduang U, Noga E (2001) Peptide antibiotics in mast cells of fish. Nature 414:268–269

    Article  CAS  PubMed  Google Scholar 

  • Smith SN, Armstrong RA, Springate J, Barker G (1985) Infection and colonization of trout eggs by Saprolegniaceae. T Brit Mycol Soc 85:719–723

    Article  Google Scholar 

  • St Mary CM, Gordon E, Hale RE (2004) Environmental effects on egg development and hatching success in Jordanella floridae, a species with parental care. J Fish Biol 65:760–768

    Article  Google Scholar 

  • Thoen E, Evensen Ø, Skaar I (2011) Pathenogenicity of Saprolegnia spp. to Atlantic salmon, Salmo salar L., eggs. J Fish Dis 34:601–608

    Article  CAS  PubMed  Google Scholar 

  • van West P (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20:99–104

    Article  Google Scholar 

  • Wackerly DD, Mendenhall W III, Schaeffer RL (2008) Mathematical statistics with applications, 7th edn. Brooks/Cole, Belmont CA

    Google Scholar 

  • Wetzel RG (1983) Limnology, 2nd edn. Saunders, New York

    Google Scholar 

  • Winn HE (1958) Observations on the reproductive habits of darters (Pisces-Percidae). Am Midl Nat 59:190–212

    Article  Google Scholar 

Download references

Acknowledgments

I am indebted to USI undergrads A. Niemeier, S. Hampton, A. White, C. Piestrup, and A. Johnson for invaluable assistance in both field and laboratory aspects of this research. W. Wilding and G. Bandoli provided statistical support. The University of Southern Indiana provided laboratory space and computing support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James H. Bandoli.

Ethics declarations

Ethical standards

This research was conducted under permit no. 2012-001 from the University of Southern Indiana Dept. of Biology Animal Care and Use Committee and complied with current laws regarding animal experimentation in the USA.

Additional information

Communicated by K. Lindström

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bandoli, J.H. Filial cannibalism in spottail darters (Etheostoma squamiceps) includes the targeted removal of infected eggs. Behav Ecol Sociobiol 70, 617–624 (2016). https://doi.org/10.1007/s00265-016-2081-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-016-2081-7

Keywords

Navigation