Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods

Abstracts

The importance of the role that parasites play in ecological communities is becoming increasingly apparent. However much about their impact on hosts and thus populations and communities remains poorly understood. A common observation in wild populations is high variation in levels of parasite infestation among hosts. While high variation could be due to chance encounter, there is increasing evidence to suggest that such patterns are due to a combination of environmental, host, and parasite factors. In order to examine the role of host condition on parasite infection, rates of Gnathia marleyi infestation were compared between experimentally injured and uninjured fish hosts. Experimental injuries were similar to the minor wounds commonly observed in nature. The presence of the injury significantly increased the probability of infestation by gnathiids. However, the level of infestation (i.e., total number of gnathiid parasites) for individual hosts, appeared to be unaffected by the treatment. The results from this study indicate that injuries obtained by fish in nature may carry the additional cost of increased parasite burden along with the costs typically associated with physical injury. These results suggest that host condition may be an important factor in determining the likelihood of infestation by a common coral reef fish ectoparasite, G. marleyi.

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References

  1. Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85(02):373–398

    Article  PubMed  Google Scholar 

  2. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions: I. Regulatory processes. J Anim Ecol 47(1):219–247

    Article  Google Scholar 

  3. Arnal C, Côté IM (2000) Diet of broadstripe cleaning gobies on a Barbadian reef. J Fish Biol 57(4):1075–1082

    Article  Google Scholar 

  4. Arnal C, Côté IM, Morand S (2001) Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behav Ecol Sociobiol 51(1):1–7

    Article  Google Scholar 

  5. Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlement-stage reef fish in the eastern Caribbean Sea. Bull Mar Sci 91(4):479–487

    Article  Google Scholar 

  6. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10(2):131–165

    Article  Google Scholar 

  7. Bereiter-Hahn J, Zylberberg L (1993) Regeneration of teleost fish scale. Comp Biochem Physiol A Physiol 105(4):625–641

    Article  Google Scholar 

  8. Blanco G, Tella JL, Potti J (1997) Feather mites on group-living red-billed choughs: a non-parasitic interaction? J Avian Biol 28(3):197–206

    Article  Google Scholar 

  9. Bunnell T, Hanisch K, Hardege JD, Breuthaupt T (2011) The fecal odor of sick hedgehogs (Erinaceus europaeus) mediates olfactory attraction of the tick Ixodes hexagonus. J Chem Ecol 37(4):340

    CAS  Article  PubMed  Google Scholar 

  10. Butcher PA, Broadhurst MK, Hall KC, Cullis BR, Nicoll RG (2009) Scale loss and mortality in angled-and-released eastern sea garfish (Hyporhamphus australis). ICES J Mar Sci 67(3):522–529

    Article  Google Scholar 

  11. Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140(07):888–896

    CAS  Article  PubMed  Google Scholar 

  12. Coile AM, Welicky RL, Sikkel PC (2014) Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol Res 113(10):3875–3880

    CAS  Article  PubMed  Google Scholar 

  13. Davies AJ, Johnston MRL (2000) The biology of some intraerythrocytic parasites of fishes, amphibia and reptiles. Adv Parasitol 45:1–107

    CAS  Article  PubMed  Google Scholar 

  14. Davies AJ, Smit NJ (2001) The life cycle of Haemogregarina bigemina (Adeleina: Haemogregarinidae) in South African hosts. Folia Parasitol 48(3):169–177

    Article  Google Scholar 

  15. Davis MW (2002) Key principles for understanding fish bycatch discard mortality. Can J Fish Aquat Sci 59(11):1834–1843

    Article  Google Scholar 

  16. Dawson RD, Bortolotti GR (1997) Are avian hematocrits indicative of condition? American kestrels as a model. J Wildl Manag 61(4):1297–1306

    Article  Google Scholar 

  17. Deveney M, Chisholm L, Whittington I (2001) First published record of the pathogenic monogenean parasite Neobenedenia melleni (Capsalidae) from Australia. Dis Aquat Organ 46:79–82

    CAS  Article  PubMed  Google Scholar 

  18. Eiras AE, Jepson PC (1991) Host location by Aedes aegypti (Diptera: Culicidae): a wind tunnel study of chemical cues. Bull Entomol Res 81(02):151–160

    Article  Google Scholar 

  19. Farquharson C, Smit NJ, Sikkel PC (2012) Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the eastern Caribbean. Zootaxa 3381(1):47–61

    Google Scholar 

  20. Ferreira ML, Smit NJ, Grutter AS, Davies AJ (2009) A new species of gnathiid (Crustacea: Isopoda) parasitizing teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol 95(5):1066–1075

    Article  PubMed  Google Scholar 

  21. Finley RJ, Forrester GE (2003) Impact of ectoparasites on the demography of a small reef fish. Mar Ecol Prog Ser 248:305–309

    Article  Google Scholar 

  22. Foster SA (1985) Wound healing: a possible role of cleaning stations. Copeia 1985(4):875–880

    Article  Google Scholar 

  23. Freestone AL, Osman RW, Ruiz GM, Torchin ME (2011) Stronger predation in the tropics shapes species richness patterns in marine communities. Ecology 92(4):983–993

    Article  PubMed  Google Scholar 

  24. González P et al (2004) A preliminary study on gill metazoan parasites of Dentex dentex (Pisces: Sparidae) from the western Mediterranean Sea (Balearic Islands). J Appl Ichthyol 20(4):276–281

    Article  Google Scholar 

  25. Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol: Prog Ser 115:21–30

    Article  Google Scholar 

  26. Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol: Prog Ser 130:61–70

    Article  Google Scholar 

  27. Grutter AS, Poulin P (1998) Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Mar Ecol: Prog Ser 164:263–271

    Article  Google Scholar 

  28. Grutter AS et al (2011) Fish mucous cocoons: the “mosquito nets” of the sea. Biol Lett 7(2):292–294

    Article  PubMed  Google Scholar 

  29. Hatcher MJ, Dunn AM (2011) Parasites in ecological communities: from interactions to ecosystems. Cambridge University Press

  30. Hayes PM, Smit NJ, Grutter AS, Davies AJ (2011) Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit. J Fish Dis 34(7):563–566

    CAS  Article  PubMed  Google Scholar 

  31. Horton T, Okamura B (2003) Post-haemorrhagic anaemia in sea bass, Dicentrarchus labrax (L.), caused by blood feeding of Ceratothoa oestroides (Isopoda: Cymothoidae). J Fish Dis 26(7):401–406

    CAS  Article  PubMed  Google Scholar 

  32. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21(7):381–385

    Article  PubMed  Google Scholar 

  33. Johnson PT et al (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25(6):362–371

    Article  PubMed  Google Scholar 

  34. Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66(3):860–864

    Article  Google Scholar 

  35. Jones CM et al (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37(8):927–935

  36. Keymer A, Crompton DWT, Walters DE (1983) Nippostrongylus (Nematoda) in protein-malnourished rats: host mortality, morbidity and rehabilitation. Parasitology 86(3):461–475

    Article  PubMed  Google Scholar 

  37. Klitgaard AB (1997) The distribution and habitats in the North Atlantic of two gnathiid species (Crustacea, Isopoda) and their reproductive biology in the Denmark Strait and north of Iceland. Meddelelser om Grønland, Bioscience 47:1–32

  38. Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73(6):1121–1128

    Article  Google Scholar 

  39. Krasnov BR, Khokhlova IS, Arakelyan MS, Degen AA (2005) Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Fungal Ecol 19(4):625–631

    Article  Google Scholar 

  40. Kuris AM, Lafferty KD (2000) Parasite-host modelling meets reality: adaptive peaks and theirecological attributes. In: Poulin R, Morand S, Skorping A (eds) Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality. Elsevier, Amsterdam 32:9–26

  41. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17(11):507–513

    Article  Google Scholar 

  42. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci 103(30):11211–11216

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Lafferty KD et al (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11(6):533–546

    Article  PubMed  PubMed Central  Google Scholar 

  44. Manship BM, Walker AJ, Davies AJ (2011) Brooding and embryonic development in the crustacean Paragnathia formica (Hesse, 1864) (Peracarida: Isopoda: Gnathiidae). Arthropod Struct Dev 40(2):135–145

    Article  PubMed  Google Scholar 

  45. Manship BM, Walker AJ, Jones LA, Davies AJ (2012) Blood feeding in juvenile Paragnathia formica (Isopoda: Gnathiidae): biochemical characterization of trypsin inhibitors, detection of anticoagulants, and molecular identification of fish hosts. Parasitology 139(6):744–754

    CAS  Article  PubMed  Google Scholar 

  46. Marcogliese DJ, Cone DK (1997) Food webs: a plea for parasites. Trends Ecol Evol 12(8):320–325

    CAS  Article  PubMed  Google Scholar 

  47. Marino F et al (2004) Tissue damage and haematophagia due to praniza larvae (Isopoda: Gnathiidae) in some aquarium seawater teleosts. Dis Aquat Organ 59(1):43–47

    CAS  Article  PubMed  Google Scholar 

  48. Nagel L, Grutter AS (2007) Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes. J Fish Biol 70(2):497–508

    Article  Google Scholar 

  49. Nagel L, Montgomerie R, Lougheed SC (2008) Evolutionary divergence in common marine ectoparasites Gnathia spp. (Isopoda: Gnathiidae) on the Great Barrier Reef: phylogeography, morphology, and behaviour. Biol J Linn Soc 94(3):569–587

    Article  Google Scholar 

  50. Ota Y, Hoshino O, Hirose M, Tanaka K, Hirose E (2012) Third-stage larva shifts host fish from teleost to elasmobranch in the temporary parasitic isopod, Gnathia trimaculata (Crustacea; Gnathiidae). Mar Biol 159(10):2333–2347

    CAS  Article  Google Scholar 

  51. Panek FM (2005) Epizootics and disease of coral reef fish in the tropical western Atlantic and Gulf of Mexico. Rev Fish Sci 13(1):1–21

    Article  Google Scholar 

  52. Poulin R (1998) Host and environmental correlates of body size in ticks (Acari: Argasidae and Ixodidae). Can J Zool 76(5):925–930

    Article  Google Scholar 

  53. Quattrini AM, Demopoulos AWJ (2016) Ectoparasitism on deep-sea fishes in the western North Atlantic: In situ observations from ROV surveys. Int J Parasitol: Parasites and Wildlife 5(3):217–228

    Google Scholar 

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

  55. Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23(11):610–618

    Article  PubMed  Google Scholar 

  56. Rohde K (2002) Ecology and biogeography of marine parasites. Adv Mar Biol 43:1–83

    Article  PubMed  Google Scholar 

  57. Rohde K et al (1998) Nestedness in assemblages of metazoan ecto-and endoparasites of marine fish. Adv Mar Biol 28(4):543–549

    CAS  Google Scholar 

  58. Rottmann RW, Francis-Floyd R, Durborow R (1992) The role of stress in fish disease. Southern Regional Aquaculture Center Pub 1992:474

  59. Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86(2):228–232

    Article  PubMed  Google Scholar 

  60. Sato T et al (2012) Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts. Ecol Lett 15(8):786–793

    Article  PubMed  Google Scholar 

  61. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11(8):317–321

    CAS  Article  PubMed  Google Scholar 

  62. Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25(4):683–689

    Article  Google Scholar 

  63. Sikkel PC, Ziemba RE, Sears WT, Wheeler JC (2009) Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28(2):489–495

    Article  Google Scholar 

  64. Sikkel PC, Sears WT, Weldon B, Tuttle BC (2011) An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod. Mar Biol 158(5):1075–1083

    Article  Google Scholar 

  65. Sikkel PC, Tuttle LJ, Cure K, Coile AM, Hixon MA (2014) Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite in both its introduced and native ranges. PloS One 9(5):e95854

    Article  PubMed  PubMed Central  Google Scholar 

  66. Sikkel PC et al (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull Mar Sci 93(2):475–489

    Article  Google Scholar 

  67. Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391

    CAS  Article  PubMed  Google Scholar 

  68. Stepien CA, Brusca RC (1985) Nocturnal Attacks on Nearshor Fishes in Southern California by crustacean zooplankton. Mar Ecol: Prog Ser 25:91–105

    Article  Google Scholar 

  69. Sukhdeo MVK, Hernandez AD (2005) Food web patterns and the parasite’s perspective. Parasitism and ecosystems. Oxford University Press, Oxford, pp 54–67

    Google Scholar 

  70. Tanaka K (2007) Life history of gnathiid isopods-current knowledge and future directions. Plankon Benthos Res 2(1):1–11

    Article  Google Scholar 

  71. Triki Z, Grutter AS, Bshary R, Ros AFH (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163(9):187

    Article  Google Scholar 

  72. Tschirren B, Bischoff LL, Saladin V, Richner H (2007) Host condition and host immunity affect parasite fitness in a bird–ectoparasite system. Funct Ecol 21(2):372–378

    Article  Google Scholar 

  73. Whiteman EA, Côté IM (2002) Cleaning activity of two Caribbean cleaning gobies: intra-and interspecific comparisons. J Fish Biol 60(6):1443–1458

    Article  Google Scholar 

  74. Wood CL et al (2007) Parasites alter community structure. Proc Natl Acad Sci 104(22):9335–9339

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  75. Zeileis A, Kleiber C, Jackman S (2008) Regression Models for Count Data in R. J Stat Softw 27:8 http://www.jstatsoft.org/v27/i08/

    Google Scholar 

  76. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26(10):1009–1024

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank members of the Sikkel lab of Arkansas State University, the Benthic Ecology lab of the USGS Wetland and Aquatic Research Center, and the staff of the Virgin Islands Environmental Resource Station (VIERS) for logistical support and use of their facilities. We would also like to thank Anne Marie Coile, Ashley Elsishans King, and Whitney Sears for assisting with data collection. A portion of the fieldwork reported herein was supported by National Science Foundation grant OCE-121615, PC Sikkel, PI, and Puerto Rico Sea Grant R-31-1-4. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government. This is contribution # 185 from the University of the Virgin Islands Center for Marine and Environmental Studies.

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Correspondence to Paul C. Sikkel.

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W. Jenkins, P. Sikkel, and A. Demopoulos declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of Arkansas State University.

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Jenkins, W.G., Demopoulos, A.W.J. & Sikkel, P.C. Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods. Symbiosis 75, 113–121 (2018). https://doi.org/10.1007/s13199-017-0518-z

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Keywords

  • Marine symbiosis
  • Host condition
  • Ectoparasite
  • Gnathiidae
  • Coral reefs