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Infections may select for filial cannibalism by impacting egg survival in interactions with water salinity and egg density

  • Behavioral ecology - Original research
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Abstract

In aquatic environments, externally developing eggs are in constant contact with the surrounding water, highlighting the significance of water parameters and pathogens for egg survival. In this study we tested the impact of water salinity, egg density and infection potential of the environment on egg viability in the sand goby (Pomatoschistus minutus), a small fish that exhibits paternal egg care and has a marine origin, but which in the Baltic Sea lives in brackish water. To manipulate the infection potential of the environment, we added either a Saprolegnia infection vector into UV-filtered water or a fungicide into natural Baltic Sea water. Saprolegnia are widely spread water moulds that are a key cause of egg mortality in aquatic organisms in fresh- and brackish water. We found that increased water salinity indeed decreased the egg infection rate and had a positive effect on egg viability, while high egg density tended to have the opposite effect. However, the different factors influenced egg viability interactively, with a higher egg density having negative effects at low, but not in high, salinity. Thus, the challenges facing marine organisms adapting to lower salinity levels can be amplified by Saprolegnia infections that reduce egg survival in interaction with other environmental factors. Our results support the hypothesis that suppressing egg infections is an important aspect of parental care that can select for filial cannibalism, a common but poorly understood behaviour, especially in fish with parental care.

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References

  • Boos S, Meunier J, Pichon S, Kölliker M (2014) Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol 25:754–761. doi:10.1093/beheco/aru046

    Article  Google Scholar 

  • Bouchereau J-L, Guelorget O (1997) Comparison of three Gobiidae (Teleostei) life history strategies over their geographical range. Oceanol Acta 21:503–517. doi:10.1016/S0399-1784(98)80034-0

    Article  Google Scholar 

  • Brown AC, Clotfelter ED (2012) Fighting fish (Betta splendens) bubble nests do not inhibit microbial growth. J Exp Zool Part A 317:481–487. doi:10.1002/jez.1740

    Article  Google Scholar 

  • Celada JD, Carral JM, Sáez-Royuela M, Melendre PM, Aguilera A (2004) Effects of different antifungal treatments on artificial incubation of the astacid crayfish (Pacifastacus leniusculus Dana) eggs. Aquaculture 239:249–259. doi:10.1016/j.aquaculture.2004.06.003

    Article  CAS  Google Scholar 

  • Chatto DA (1979) Effects of salinity on hatching success of the sui-ui. Prog Fish Cult 41:82–85. doi:10.1577/1548-8659(1979)41[82:EOSOHS]2.0.CO;2

  • Chin-Baarstad A, Klug H, Lindström K (2009) Should you eat your offspring before someone else does? Effect of an egg predator on filial cannibalism in the sand goby. Anim Behav 78:203–208. doi:10.1016/j.anbehav.2009.04.022

    Article  Google Scholar 

  • Clark L, Mason JR (1985) Use of nest material as insecticidal and antipathogenic agents by the European starling. Oecologia 67:169–176. doi:10.1007/BF00384280

    Article  Google Scholar 

  • Côté IM, Gross MR (1993) Reduced disease in offspring—a benefit of coloniality in sunfish. Behav Ecol Sociobiol 33:269–274. doi:10.1007/BF02027124

    Article  Google Scholar 

  • Defaveri J, Merilä J (2013) Local adaptation to salinity in the three-spined stickleback? J Evol Biol 27:290–302. doi:10.1111/jeb.12289

    Article  PubMed  Google Scholar 

  • Edgell P, Lawseth D, McLean WE, Britton EW (1993) The use of salt solutions to control fungus (Saprolegnia) infestations on salmon eggs. Prog Fish Cult 55:48–52. doi:10.1577/1548-8640(1993)055<0048:TUOSST>2.3.CO;2

    Article  Google Scholar 

  • Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X (2001) Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122:563–569. doi:10.1017/S0031182001007740

    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. doi:10.1007/s00442-010-1889-5

    Article  PubMed  Google Scholar 

  • Fonds M (1973) Sand gobies in the Dutch Wadden Sea (Pomatoschistus, Gobiidae, Pisces). Neth J Sea Res 6:417–478. doi:10.1016/0077-7579(73)90001-X

    Article  Google Scholar 

  • Fonds M, Van Buurt G (1974) The influence of temperature and salinity on development and survival of goby eggs (Pisces, Gobiidae). Hydrobiol Bull 8:110–116. doi:10.1007/BF02254911

    Article  Google Scholar 

  • Forsgren E (1999) Sexual selection and sex roles in the sand goby. In: Almada VC, Oliveira RF, Gonçalves EJ (eds) Behaviour and conservation of littoral fishes. Instituto Superior de Psicologia Aplicada, Lisbon, pp 249–274

    Google Scholar 

  • Forsgren E, Kvarnemo C, Lindström K (1996) Mode of sexual selection determined by resource abundance in two sand goby populations. Evolution 50:646–654

    Article  Google Scholar 

  • Gerking SD, Lee RM (1980) Reproductive performance of the desert pupfish (Cyprinodon n. nevadensis) in relation to salinity. Environ Biol Fish 5:375–378. doi:10.1007/BF00005190

    Article  Google Scholar 

  • Giacomello E, Marri L, Marchini D, Mazzoldi C, Rasotto MB (2008) Sperm-duct gland secretion of the grass goby Zosterisessor ophiocephalus exhibits antimicrobial activity. J Fish Biol 73:1823–1828. doi:10.1111/j.1095-8649.2008.02069.x

    Article  Google Scholar 

  • Hale RE (2008) Evidence that context-dependent mate choice for parental care mirrors benefits to offspring. Anim Behav 75:1283–1290. doi:10.1016/j.anbehav.2007.09.034

    Article  Google Scholar 

  • Heikkinen J, Mustonen SM, Eskelinenc P, Sundbergd L-R, Von Wright A (2013) Prevention of fungal infestation of rainbow trout (Oncorhynchus mykiss) eggs using UV irradiation of the hatching water. Aquacult Eng 55:9–15. doi:10.1016/j.aquaeng.2013.01.001

    Article  Google Scholar 

  • Hesthagen IH (1977) Migrations, breeding and growth in Pomatoschistus minutus (Pallas) (Pisces, Gobiidae) in Oslofjorden, Norway. Sarsia 63:17–26

    Google Scholar 

  • Hussein MMA, Hatai K (2002) Pathogenicity of Saprolegnia species associated with outbreaks of salmonid saprolegniosis in Japan. Fish Sci 68:1067–1072

    Article  CAS  Google Scholar 

  • Jansson B-O, Aneer G, Nellbring S (1985) Spatial and temporal distribution of the demersal fish fauna in a Baltic archipelago as estimated by SCUBA census. Mar Ecol Prog Ser 23:31–43

    Article  Google Scholar 

  • Japoshvili B, Lehtonen TK, Wong BBM, Lindström K (2012) Repeatability of nest size choice and nest building in sand gobies. Anim Behav 84:913–917. doi:10.1016/j.anbehav.2012.07.015

    Article  Google Scholar 

  • Järvi-Laturi M, Lehtonen TK, Pampoulie C, Lindström K (2008) Parental care behaviour of sand gobies is determined by habitat related nest structure. Behaviour 145:39–50. doi:10.1163/156853908782687197

    Article  Google Scholar 

  • Karås P, Klingsheim V (1997) Effects of temperature and salinity on embryonic development of turbot (Scophthalmus maximus L.) from the North Sea, and comparisons with Baltic populations. Helgoländer Meeresun 51:241–247. doi:10.1007/BF02908710

    Article  Google Scholar 

  • Kitancharoen N, Hatai K, Yamamoto A (1997) Aquatic fungi developing on eggs of Salmonids. J Aquat Anim Health 9:314–316. doi:10.1577/1548-8667(1997)009<0314:AFDOEO>2.3.CO;2

    Article  Google Scholar 

  • Klug H, Lindström K (2008) Hurry-up and hatch: selective filial cannibalism of slower developing eggs. Biol Lett 4:160–162. doi:10.1098/rsbl.2007.0589

    Article  PubMed Central  PubMed  Google Scholar 

  • Klug H, Lindström K, St Mary CM (2006) Parents benefit from eating offspring: density-dependent egg survivorship compensates for filial cannibalism. Evolution 60:2087–2095. doi:10.1111/j.0014-3820.2006.tb01846.x

    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. doi:10.1098/rspb.2003.2501

    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. doi:10.1016/0376-6357(95)00019-4

    Article  CAS  Google Scholar 

  • Kvarnemo C (1994) Temperature differentially affects male and female reproductive rates in the sand goby: consequences for operational sex ratio. Proc R Soc Lond B 256:151–156. doi:10.1098/rspb.1994.0063

    Article  Google Scholar 

  • Lategan MJ, Torpy FR, Gibson LF (2004) Biocontrol of saprolegniosis in silver perch Bidyanus bidyanus (Mitchell) by Aeromonas media strain A199. Aquaculture 235:77–88. doi:10.1016/j.aquaculture.2003.09.014

    Article  Google Scholar 

  • Lehtonen TK (2012) Signal value of male courtship effort in a fish with paternal care. Anim Behav 83:1153–1161. doi:10.1016/j.anbehav.2012.01.040

    Article  Google Scholar 

  • Lehtonen T, Lindström K (2004) Changes in sexual selection resulting from novel habitat use in the sand goby. Oikos 104:327–335. doi:10.1111/j.0030-1299.2004.12489.x

    Article  Google Scholar 

  • Lehtonen TK, Lindström K (2007) Mate compatibility, parental allocation and fitness consequences of mate choice in the sand goby Pomatoschistus minutus. Behav Ecol Sociobiol 61:1581–1588. doi:10.1007/s00265-007-0390-6

    Article  Google Scholar 

  • Lindström K (1998) Effects of costs and benefits of brood care on filial cannibalism in the sand goby. Behav Ecol Sociobiol 42:101–106. doi:10.1007/s002650050417

    Article  Google Scholar 

  • Lissåker M, Svensson O (2008) Cannibalize or care? The role of perceived paternity in the sand goby, Pomatoschistus minutus. Behav Ecol Sociobiol 62:1467–1475. doi:10.1007/s00265-008-0576-6

    Article  Google Scholar 

  • Lissåker M, Kvarnemo C, Svensson O (2003) Effects of a low oxygen environment on parental effort and filial cannibalism in the male sand goby, Pomatoschistus minutus. Behav Ecol 14:374–381. doi:10.1093/beheco/14.3.374

    Article  Google Scholar 

  • Little TJ, Perutz M, Palmer M, Crossan C, Braithwaite VA (2008) Male three-spined sticklebacks Gasterosteus aculeatus make antibiotic nests: a novel form of parental protection? J Fish Biol 73:2380–2389. doi:10.1111/j.1095-8649.2008.02086.x

    Article  Google Scholar 

  • Marchinko KB, Schluter D (2007) Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 61:1084–1090. doi:10.1111/j.1558-5646.2007.00103.x

    Article  PubMed  Google Scholar 

  • Marking LL, Rach JJ, Schreier TM (1994) American Fisheries Society evaluation of antifungal agents for fish culture. Prog Fish Cult 56:225–231. doi:10.1577/1548-8640(1994)056<0225:AFSEOA>2.3.CO;2

    Article  Google Scholar 

  • Meier HEM (2006) Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim Dynam 27:39–68. doi:10.1007/s00382-006-0124-x

    Article  Google Scholar 

  • Miller PJ (1986) Gobiidae. In: Whitehead PJP (ed) Fishes of the north-eastern Atlantic and the Mediterranean, vol3. UNESCO, Paris, pp 1019–1085

    Google Scholar 

  • Neumann T (2010) Climate-change effects on the Baltic Sea ecosystem: a model study. J Mar Syst 81:213–224. doi:10.1016/j.jmarsys.2009.12.001

    Article  Google Scholar 

  • Nissling A, Dahlman G (2010) Fecundity of flounder, Pleuronectes flesus, in the Baltic Sea—reproductive strategies in two sympatric populations. J Sea Res 64:190–198. doi:10.1016/j.seares.2010.02.001

    Article  Google Scholar 

  • Nissling A, Westin L, Hjerne O (2002) Reproductive success in relation to salinity for three flatfish species, dab (Limanda limanda), plaice (Pleuronectes platessa), and flounder (Pleuronectes flesus), in the brackish water Baltic Sea. ICES J Mar Sci 59:93–108. doi:10.1006/jmsc.2001.1134

    Article  Google Scholar 

  • Nissling A, Johansson U, Jacobsson M (2006) Effects of salinity and temperature conditions on the reproductive success of turbot (Scophthalmus maximus) in the Baltic Sea. Fish Res 80:230–238. doi:10.1016/j.fishres.2006.04.005

    Article  Google Scholar 

  • Norevik Andrén M, Kvarnemo C (2014) Filial cannibalism in a nest-guarding fish: females prefer to spawn in nests with few eggs over many. Behav Ecol Sociobiol 68:1565–1576. doi:10.1007/s00265-014-1766-z

    Article  Google Scholar 

  • Padgett DE (1978) Salinity tolerance of an isolate of Saprolegnia australis. Mycologia 70:1288–1293

    Article  Google Scholar 

  • Pampoulie C, Lindström K, St Mary CM (2004) Have your cake and eat it too: male sand gobies show more parental care in the presence of female partners. Behav Ecol 15:199–204. doi:10.1093/beheco/arg107

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Racha JJ, Valentine JJ, Schreier TM, Gaikowski MP, Crawford TG (2004) Efficacy of hydrogen peroxide to control saprolegniasis on channel catfish (Ictaluruspunctatus) eggs. Aquaculture 238:135–142. doi:10.1016/j.aquaculture.2004.06.007

    Article  Google Scholar 

  • Rasowo J, Okoth OE, Ngugi CC (2007) Effects of formaldehyde, sodium chloride, potassium permanganate and hydrogen peroxide on hatch rate of African catfish Clarias gariepinus eggs. Aquaculture 269:271–277. doi:10.1016/j.aquaculture.2007.04.087

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rushbrook BJ, Barber I (2008) A comparison of nest building by three-spined sticklebacks Gasterosteus aculeatus from still and flowing waters. J Fish Biol 73:746–752. doi:10.1111/j.1095-8649.2008.01970.x

    Article  Google Scholar 

  • Sagvik J, Uller T, Stenlund T, Olsson M (2008) Intraspecific variation in resistance of frog eggs to fungal infection. Evol Ecol 22:193–201. doi:10.1007/s10682-007-9168-6

    Article  Google Scholar 

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

    Google Scholar 

  • Schreier TM, Rach JJ, Howe GE (1996) Efficacy of formalin, hydrogen peroxide, and sodium chloride on fungal-infected rainbow trout eggs. Aquaculture 140:323–331. doi:10.1016/0044-8486(95)01182-X

    Article  CAS  Google Scholar 

  • Singer A, Kvarnemo C, Lindström K, Svensson O (2006) Genetic mating patterns studied in pools with manipulated nest site availability in two populations of Pomatoschistus minutus. J Evol Biol 19:1641–1650. doi:10.1111/j.1420-9101.2006.01114.x

    Article  CAS  PubMed  Google Scholar 

  • Smith SN, Armstrong RA, Springate J, Barker G (1985) Infection and colonization of trout eggs by Saprolegniaceae. Trans Brit Mycol Soc 85:719–764. doi:10.1016/S0007-1536(85)80268-0

    Article  Google Scholar 

  • St Mary CM, Noureddine CG, Lindström K (2001) Effects of the environment on male reproductive success and parental care in the Florida flagfish, Jordanella floridae. Ethology 107:1035–1052. doi:10.1046/j.1439-0310.2001.00747.x

    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. doi:10.1111/j.1095-8649.2004.00481.x

    Article  Google Scholar 

  • Sundell J (1994) Dynamics and composition of littoral fish fauna along the coast of SW-Finland. Aqua Fenn 24:37–49

    Google Scholar 

  • Taylor SG, Bailey JE (1979) Saprolegnia—control of fungus on incubating eggs of pink salmon by treatment with seawater. Prog Fish Cult 41:181–183. doi:10.1577/1548-8659(1979)41[181:S]2.0.CO;2

  • Thoen E, Evensen Ø, Skaar I (2011) Pathogenicity of Saprolegnia spp. to Atlantic salmon, Salmo salar L., eggs. J Fish Dis 34:601–608. doi:10.1111/j.1365-2761.2011.01273.x

    Article  CAS  PubMed  Google Scholar 

  • Thorsen A, Kjesbu OS, Fyhn HJ, Solemdal P (1996) Physiological mechanisms of buoyancy in eggs from brackish water cod. J Fish Biol 48:457–477. doi:10.1111/j.1095-8649.1996.tb01440.x

    Article  CAS  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. doi:10.1016/j.mycol.2006.06.004

    Article  Google Scholar 

  • Westman P, Sohlenius G (1999) Diatom stratigraphy in five offshore sediment cores from the northwestern Baltic proper implying large scale circulation changes during the last 8,500 years. J Paleolimnol 22:53–69. doi:10.1023/A:1008011511101

    Article  Google Scholar 

  • Wikner J, Andersson A (2012) Increased freshwater discharge shifts the trophic balance in the coastal zone of the northern Baltic Sea. Glob Change Biol 18:2509–2519. doi:10.1111/j.1365-2486.2012.02718.x

    Article  Google Scholar 

  • Wimberger PH (1984) The use of green plant material in bird nests to avoid ectoparasites. Auk 101:615–618

    Google Scholar 

  • Winn HE (1958) Comparative reproductive behavior and rcology of fourteen species of darters (Pisces-Percidae). Ecol Monogr 28:155–191

    Article  Google Scholar 

  • Wong BBM, Lehtonen TK, Lindström K (2008) Male nest choice in sand gobies, Pomatoschistus minutus. Ethology 114:575–581. doi:10.1111/j.1439-0310.2008.01500.x

    Article  Google Scholar 

  • Zander CD (1990) Habitat and prey dependant distribution of sand gobies, Pomatoschistus minutus (Gobiidae, Teleostei) in the SW Baltic. Zool Anz 224:328–341

    Google Scholar 

  • Zuur AF, Hilbe J, Ieno EN (2013) A beginner’s guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists. Highland Statistics, Newburgh

    Google Scholar 

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Acknowledgements

We thank Anniina Saarinen, Emilie Suominen and Jolanda Linsén for their invaluable help with maintaining the fish and their eggs, Ola Svensson for inspiring discussions and comments on the manuscript, Kai Lindström for the loan of equipment and Jaana Koistinen, Joanna Norkko and the rest of the helpful staff of the Tvärminne Zoological Station for logistic support. TKL was funded by the Department of Biology, University of Turku. CK thanks the Swedish Research Council for funding (Grant 621-2011-4004). This work is part of that of the Linnaeus Centre for Marine Evolutionary Biology (CeMEB).

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None.

Ethical standard

All applicable national guidelines for the care and use of animals were followed. The experimental procedures were approved by ELLA—the National Animal Experiment Board of Finland.

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Authors and Affiliations

  1. Department of Biosciences, Åbo Akademi University, Tykistökatu 6, 20520, Turku, Finland

    Topi K. Lehtonen & Charlotta Kvarnemo

  2. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

    Topi K. Lehtonen

  3. Department of Biology and Environmental Sciences, University of Gothenburg, Box 463, 40530, Gothenburg, Sweden

    Charlotta Kvarnemo

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  1. Topi K. Lehtonen
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Correspondence to Topi K. Lehtonen.

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Communicated by Joel Trexler.

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Lehtonen, T.K., Kvarnemo, C. Infections may select for filial cannibalism by impacting egg survival in interactions with water salinity and egg density. Oecologia 178, 673–683 (2015). https://doi.org/10.1007/s00442-015-3246-1

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