Abstract
The density-dependent prophylaxis hypothesis predicts that individuals at high density will invest more resources into immune defence than individuals at lower densities as a counter-measure to density-dependent pathogen transmission rates. Evidence has been found for this hypothesis in insects, but not in a non-arthropod taxon. To investigate this hypothesis in the coral-eating crown-of-thorns sea star, Acanthaster planci, density treatments were set up over 21 days, and pathogen infection was simulated with bacterial injection. Five immune responses: amoebocyte count, amoebocyte viability, lysosomal membrane integrity, respiratory burst and peroxidase activity were all upregulated at high density. These results demonstrate that immune investment shows phenotypic plasticity with adult population density in agreement with the density-dependent prophylaxis hypothesis. Here I show that the density-dependent prophylaxis hypothesis is neither dependent on larval density nor restricted to insects, and hence may potentially have important consequences on disease dynamics in any species with widely fluctuating population densities. This is the first demonstration of the density-dependent prophylaxis hypothesis outside arthropods.
References
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383
Anderson RM, May RM (1979) Population biology of infectious diseases. Nature 280:361–367
Anderson RM, May RM (1981) The population dynamics of micro-parasites and their invertebrate hosts. Philos Trans R Soc Lond B Biol Sci 291:451–524
Babior M (1984) The respiratory burst of phagocytes. J Clin Investig 73:599–601
Barnes AI, Siva-Jothy MT (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc R Soc Lond B Biol Sci 267:177–182
Bekri K, Pelletier E (2004) Trophic transfer and in vivo immunotoxicological effects of tributyltin (TBT) in polar seastar Leptasterias polaris. Aquat Toxicol 66:39–53
Boman HG, Hultmark D (1987) Cell-free immunity in insects. Annu Rev Microbiol 41:103–126
Bowden TJ, Thompson KD, Morgan AL, Gratacap RML, Nikoskelainen S (2007) Seasonal variation and the immune response: A fish perspective. Fish Shellfish Immunol 22:695–706
Branham JM, Reed SA, Bailey JH, Caperon J (1971) Coral eating sea stars Acanthaster planci in Hawaii. Science 172:1155–1157
Brown CR, Brown MB (1986) Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67:1206–1218
Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 2:e711
Canicatti C (1990) Lysosomal enzyme pattern in Holothuria polii coelomocytes. J Invertebr Pathol 56:70–74
Chia FS, Xing J (1996) Echinoderm coelomocytes. Zool Stud 35:231–254
Chiu CH, Guu YK, Liu CH, Pan TM, Cheng W (2007) Immune responses and gene expression in white shrimp, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish Shellfish Immunol 23:364–377
Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592–1605
Coteur G, DeBecker G, Warnau M, Jangoux M, Dubois P (2002) Differentiation of immune cells challenged by bacteria in the common European starfish, Asterias rubens (Echinodermata). Eur J Cell Biol 81:413–418
Coteur G, Gillan D, Joly G, Pernet P, Dubois P (2003) Field contamination of the starfish Asterias rubens by metals. Part 2: Effects on cellular immunity. Environ Toxicol Chem 22:2145–2151
Cotter SC, Hails RS, Cory JS, Wilson K (2004) Density dependent prophylaxis and condition-dependent immune function in Lepidopteran larvae: a multivariate approach. J Anim Ecol 73:282–293
Dwyer G, Elkinton JS (1993) Using simple-models to predicts virus epizootics in gypsy-moth populations. J Anim Ecol 62:1–11
Endean R (1974) Acanthaster planci on the Great Barrier Reef. Proc 2nd Int Coral Reef Symp 1:563–576
Fabricius KE, Okaji K, De’ath G (2010) Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29:593–605
Freeland WJ (1979) Primate social groups as biological islands. Ecology 60:719–728
Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643
Gross PS, Al-Sharif WZ, Clow LA, Smith LC (1999) Echinoderm immunity and the evolution of the complement system. Dev Comp Immunol 23:429–442
Halliwell B, Gutteridge JMC (1998) Free radicals in biology and medicine. Clarendon Press, Oxford
Harding JM, Couturier C, Parsons GJ, Ross NW (2004a) Evaluation of the neutral red retention assay as a stress response indicator in cultivated mussels (Mytilus spp.) in relation to seasonal and environmental conditions. J Shellfish Res 23:745–751
Harding JM, Couturier C, Parsons GJ, Ross NW (2004b) Evaluation of the neutral red assay as a stress response indicator in cultivated mussels (Mytilus spp.) in relation to seasonal and environmental conditions. Aquaculture 231:315–326
Hoogland JL (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp) coloniality. Behaviour 69:1–35
Jans D, Dubois P, Jangoux M (1996) Defensive mechanisms of holothuroids (Echinodermata): formation, role, and fate of intracoelomic brown bodies in the sea cucumber Holothuria tubulosa. Cell Tissue Res 283:99–106
Kayal M, Lenihan HS, Pau C, Penin L, Adjeroud M (2011) Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak. Coral Reefs 30:827–837
Knell RJ, Begon M, Thompson DJ (1996) Transmission dynamics of Bacillus thuringiensis infecting Plodia interpunctella: a test of the mass action assumption with an insect pathogen. Proc R Soc Lond B Biol Sci 263:75–81
Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280
Kudryavtsev IV, D’Yachkov IS, Kazakov AA, Kanaikin DP, Kharazova AD, Polevshchikov AV (2005) Cellular responses of congenital immunity in the starfish Asterias rubens. J Evol Biochem Physiol 41:134–142
Kunimi Y, Yamada E (1990) Relationship of larval phase and susceptibility of the armyworm, Pseudaletia separata Walker (Lepidoptera, Nocturidae) to a nuclear polyhedrosis virus and a granulosis virus. Appl Entomol Zool 25:289–297
Kurtz J, Wiesner A, Gotz P, Sauer KP (2000) Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Dev Comp Immunol 24:1–12
Lafferty KD (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl 14:1566–1573
Lafferty KD, Kuris AM (1993) Mass mortality of abalone Haliotis cracherodii on the California Channel Islands: tests of epidemiological hypotheses. Mar Ecol Prog Ser 96:239–248
Lessells CM (2008) Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity? Philos Trans R Soc Lond B Biol Sci 363:1589–1598
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annu Rev Ecol Syst 19:371–393
Lindsey E, Mehta M, Dhulipala V, Oberhauser K, Altizer S (2009) Crowding and disease: effects of host density on response to infection in a butterfly-parasite infection. Ecol Entomol 34:551–561
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98
Lowe DM, Soverchia C, Moore MN (1995a) Lysosomal membrane responses in the blood and digestive cells of mussels experimentally exposed to fluoranthene. Aquat Toxicol 33:105–112
Lowe DM, Fossato VU, Depledge MH (1995b) Contaminant induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from Venice Lagoon: an in vitro study. Mar Ecol Prog Ser 129:189–196
McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modeled? Trends Ecol Evol 16:295–300
Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173:475–487
Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Poikonen T (2010) Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution 64:166–179
Mitsui J, Kunimi Y (1988) Effect of larval phase on susceptibility of the armyworm, Pseudaletia separata Walker (Lepidoptera, Noctuidae) to an entomogeneous Deuteromycete, Nomuraea rileyi. Jpn J Appl Entomol Zool 32:129–134
Møller AP, Dufva R, Allander K (1993) Parasites and the evolution of host social behavior. Adv Study Behav 22:65–102
Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford, UK
Moran PJ (1986) The Acanthaster phenomenon. Oceanogr Mar Biol Annu Rev 24:379–480
Moreno-Garcia M, Lanz-Mendoza H, Cordoba-Aguilar A (2010) Genetic variance and genotype-by-environment interaction of immune response in Aedes aegypti (Diptera: Culicida). J Med Entomol 47:111–120
Munoz M, Cedeno R, Rodriguez J, Van der Knaap WPW, Mialhe E, Bachere E (2000) Measurement of reactive oxygen intermediate production in haemocyte of the penaeid shrimp, Penaeus vannamei. Aquaculture 191:89–107
Newman RA (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42:671–678
Noel D, Bachere E, Mialhe E (1993) Phagocytosis associated chemiluminescence of hemocytes in Mytilus edulis (Bivalvia). Dev Comp Immunol 17:483–493
Oliver LM, Fisher WS (1999) Appraisal of prospective bivalve immunomarkers. Biomarkers 4:510–530
Papas AM (1999) Antioxidant status, diet, nutrition and health. CRC Press, Johnson City, TN
Pratchett MS (2005) Dynamics of an outbreak population of Acanthaster planci at Lizard Island, northern Great Barrier Reef (1995–1999). Coral Reefs 24:453–462
Ramírez-Gómez F, García-Arrarás JE (2010) Echinoderm immunity. Invert Survival J 7:211–220
Reeson AF, Wilson K, Gunn A, Hails RS, Goulson D (1998) Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc R Soc Lond B Biol Sci 265:1787–1791
Reeson AF, Wilson K, Cory JS, Hankard P, Weeks JM, Goulson D, Hails RS (2000) Effects of phenotypic plasticity on pathogen transmission in the field in a Lepidoptera-NPV system. Oecologia 124:373–380
Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301:472–475
Ruiz-Gonzalez MX, Moret Y, Brown MJF (2009) Rapid induction of immune density-dependent prophylaxis in adult social insects. Biol Lett 5:781–783
Schroderus E, Jokinen I, Koivula M, Koskela E, Mappes T, Mills SC, Oksanen TA, Poikonen T (2010) Common genetic basis of the endocrine and immune system in a polygynous vertebrate. Am Nat 176:E90–E97
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Shields WM, Crook JR (1987) Barn swallow coloniality – a net cost for group breeding in the Adirondacks. Ecology 68:1373–1386
Simpson SJ, Despland E, Hagele BF, Dodgson T (2001) Gregarious behavior in desert locusts is evoked by touching their back legs. Proc Natl Acad Sci USA 98:3895–3897
Smith LC, Ghosh J, Buckley KM, Clow LA, Dheilly NM, Haug T, Henson JH, Li C, Lun CM, Majeske AJ, Matranga V, Nair SV, Rast JP, Raftos DA, Roth M, Sacchi S, Schrankel CS, Stensvag K (2010) Echinoderm immunity. In: Söderhäll K (ed) Invertebrate immunity. Landes Bioscience Austin, Tex; and Springer Science, New York, NY, pp 260–301
Song YL, Hsieh YT (1994) Immunostimulation of tiger shrimp (Penaeus monodon) hemocytes for generation of microbiocidal substances: analysis of reactive oxygen species. Dev Comp Immunol 18:201–209
Song L, Li XX, Clarke S, Wang T, Bott K (2007) The application of neutral red retention assay to evaluate the differences in stress responses to sexual maturation and spawning between different sizes of Pacific oyster, Crassostrea gigas (Thunberg). J Shellfish Res 26:493–499
Stearns SC (1976) Life-history tactics - review of ideas. Q Rev Biol 51:3–47
Stearns SC (1989a) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stearns SC (1989b) The evolutionary significance of phenotypic plasticity - phenotypic sources of variation among organisms can be described by developmental switches and reaction norms. Bioscience 39:436–445
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Steinhaus EA (1958) Crowding as a possible stress factor in insect disease. Ecology 39:503–514
Uthicke S, Schaffelke B, Byrne M (2009) A boom-bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24
Vanden Bossche J-P, Jangoux M (1976) Epithelial origin of starfish coelomocytes. Nature 26:227–228
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: Consensus and controversy. Trends Ecol Evol 10:212–217
Vilmos P, Kurucz E (1998) Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol Lett 62:59–66
Webster JP, Woolhouse MEJ (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proc R Soc Lond B Biol Sci 266:391–396
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
Wilson K, Cotter SC (2008) Density-dependent prophylaxis in insects. In: Ananthakrishnan TN, Whitman DW (eds) Insects and phenotypic plasticity: Mechanisms and consequences. Science Publishers Inc, Plymouth, UK, pp 137–176
Wilson K, Reeson AF (1998) Density-dependent prophylaxis: Evidence from Lepidoptera-baculovirus interactions? Ecol Entomol 23:100–101
Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649
Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL (2002) Coping with crowds: Density-dependent disease resistance in desert locusts. Proc Natl Acad Sci USA 99:5471–5475
Yamaguchi M (1986) Acanthaster planci infestations of reefs and coral assemblages in Japan - a retrospective analysis of control effects. Coral Reefs 5:23–30
Yui MA, Bayne CJ (1983) Echinoderm immunology: Bacterial clearance by the sea urchin Strongylocentrotus purpuratus. Biol Bull 165:478–486
Acknowledgments
Thanks to CRIOBE for housing this study in their facilities, Ricardo Beldade and Gary Longo for collecting specimens, Gaël Simon and Benoit Espiau for laboratory assistance at CBETM and CRIOBE, respectively, and students and volunteers from Planete Urgence at CRIOBE for their help with the fieldwork. This research was supported by grants from ANR (ANR-06-JCJC-0012-01 and ANR-12-JCJC-Live and Let Die) and Partnership University Fund of the French American Cultural Exchange.
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Mills, S.C. Density-dependent prophylaxis in the coral-eating crown-of-thorns sea star, Acanthaster planci . Coral Reefs 31, 603–612 (2012). https://doi.org/10.1007/s00338-012-0883-2
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DOI: https://doi.org/10.1007/s00338-012-0883-2