Marine Biodiversity

, Volume 49, Issue 1, pp 83–96 | Cite as

Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines

  • T. R. N. Santos
  • P. C. SikkelEmail author
Original Paper


Gnathiid isopods are among the most common ectoparasitic organisms infesting marine fishes in benthic marine environments, and are best known in coral reef ecosystems. These micropredators are ecologically important, as they can impact their hosts directly through blood loss and tissue damage, and indirectly by transmitting blood parasites. Their abundance, and thus expected impact on hosts, varies greatly over multiple spatial scales. Most studies on gnathiids in coral reef systems have been conducted in the Caribbean and on the Great Barrier Reef, Australia, with few studies conducted in the heart of marine biodiversity, the “Coral Triangle”. This is the first field study of gnathiid ecology in the Philippines. The primary goals of this study were to characterize substrate associations and diel activity patterns of gnathiids in shallow reef areas. Gnathiid larvae were found to infest at least 28 species of hosts and were found in both seagrass and reef habitats. Within reef habitat, there was a significant difference in gnathiid abundance among coral reef substrates. Gnathiid larvae were most abundant in coral rubble substrates and least abundant on live hard coral. This is in spite of host abundance (fish) being greater near live coral. More and larger-sized gnathiids were collected from dusk to dawn compared to daytime, and gnathiids were able to find hosts using non-visual sensory cues. Our results are, thus, consistent with previous studies in the Caribbean.


Ectoparasite Micropredator Coral reef Coral Triangle Diel activity 



The authors thank the late Mayor Emmanuel Diputado, the Department of Agriculture and the Bantay Dagat of the Sibulan Municipality for logistic support and permitting access to the marine sanctuary of Agan-an. We also thank the director, Dr. Hilconida P. Calumpong, Dr. Janet S. Estacion, Dr. Rene A. Abesamis, and the staff of Silliman University Institute for Environmental and Marine Sciences for assistance and use of lab space. We thank Dianne Mira Yap, Danielle Mark Fukuda, Jean Asuncion Utzurrum, Floramae Joyce Neri, Denzyl Divinagracia, Persie Mark Sienes, and Mary Shodipo for the field assistance. Finally, we thank Dioscoro Inocencio, Rafael Ceriales, Andres B. Tubat, Paseo Tubat, and Jose G. Somoza Sr. for fish collections and field support, and Nico J. Smit for assistance with gnathiid species identification. This work was funded in part by the US National Science Foundation (OCE-1536794, PC Sikkel, PI).

Compliance with ethical standards

Ethical approval

The use and care of animals used in this study was approved by the Arkansas State University Institutional Animal Care and Use Committee (IACUC) protocol number 778227-1. All other applicable international, national, and institutional guidelines for the care and use of animals were followed.


  1. Abesamis RA, Russ GR (2005) Density-dependent spillover from a marine reserve: long-term evidence. Ecol Appl 15:1798–1812. doi: 10.1890/05-0174 CrossRefGoogle Scholar
  2. Abesamis RA, Russ GR (2010) Patterns of recruitment of coral reef fishes in a monsoonal environment. Coral Reefs 29:911–921. doi: 10.1007/s00338-010-0653-y CrossRefGoogle Scholar
  3. Abesamis RA, Stockwell BL, Bernardo LP, Villanoy CL, Russ GR (2016) Predicting reef fish connectivity from biogeographic patterns and larval dispersal modelling to inform the development of marine reserve networks. Ecol Indic 66:534–544. doi: 10.1016/j.ecolind.2016.02.032 CrossRefGoogle Scholar
  4. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42Google Scholar
  5. Alcala AC (2004) Marine reserves as tool for fishery management and biodiversity conservation: natural experiments in the central Philippines, 1974–2000. Silliman University-Angelo King Center for Research and Environmental Management, Dumaguete CityGoogle Scholar
  6. Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM (2009) Food web topology and parasites in the pelagic zone of a subarctic lake. J Anim Ecol 78:563–572. doi: 10.1111/j.1365-2656.2008.01518.x CrossRefGoogle Scholar
  7. Arnal C, Côté IM (2000) Diet of broadstripe cleaning gobies on a Barbadian reef. J Fish Biol 57:1075–1082. doi: 10.1111/j.1095-8649.2000.tb02213.x CrossRefGoogle Scholar
  8. Arneberg P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25:88–94. doi: 10.1034/j.1600-0587.2002.250110.x CrossRefGoogle Scholar
  9. Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlement-stage reef fish in the eastern Caribbean Sea. Bull Mar Sci 91:479–487. doi: 10.5343/bms.2015.1023 CrossRefGoogle Scholar
  10. Artim JM, Sikkel PC (2013) Live coral repels a common reef fish ectoparasite. Coral Reefs 32:487–494. doi: 10.1007/s00338-012-0995-8 CrossRefGoogle Scholar
  11. Bunkley-Williams L, Williams EH (1998) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–889. doi: 10.2307/3284615 CrossRefGoogle Scholar
  12. Calumpong HP, Estacion JS, Lepiten MV, Acedo CE (eds) (1997) Status of the coastal resources of the Negros learning site (Manjuyod to Dauin). Silliman University Marine Laboratory, Dumaguete City. COE-CRM document no. 1/97Google Scholar
  13. Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environ Biol Fish 72:467–480. doi: 10.1007/s10641-004-3154-4 CrossRefGoogle Scholar
  14. Chambers SD, Sikkel PC (2002) Diel emergence patterns of ecologically important, fish-parasitic, gnathiid isopod larvae on Caribbean coral reefs. Caribb J Sci 38:37–43Google Scholar
  15. Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165. doi: 10.1098/rsbl.2004.0288 CrossRefGoogle Scholar
  16. Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896. doi: 10.1017/S0031182013000097 CrossRefGoogle Scholar
  17. Cook CA, Sikkel PC, Renoux LP, Smit NJ (2015) Blood parasite biodiversity of reef-associated fishes of the eastern Caribbean. Mar Ecol Prog Ser 533:1–13. doi: 10.3354/meps11430 CrossRefGoogle Scholar
  18. Côté IM, Molloy PP (2003) Temporal variation in cleanerfish and client behaviour: does it reflect ectoparasite availability? Ethology 109:487–499. doi: 10.1046/j.1439-0310.2003.00883.x CrossRefGoogle Scholar
  19. Cruz-Lacierda ER, Nagasawa K (2017) Occurrence of praniza larvae of a gnathiid (Isopoda, Gnathiidae) on wild-caught orange-spotted grouper, Epinephelus coioides (Hamilton, 1822) (Perciformes, Serranidae), in Lingayen Gulf, Philippines. Crustaceana 90:101–110. doi: 10.1163/15685403-00003626 CrossRefGoogle Scholar
  20. Curtis LM, Grutter AS, Smit NJ, Davies AJ (2013) Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Int J Parasitol 43:361–370. doi: 10.1016/j.ijpara.2012.11.012 CrossRefGoogle Scholar
  21. Davies AJ, Smit NJ, Hayes PM, Seddon AM, Wertheim DF (2004) Haemogregarina bigemina (Protozoa: Apicomplexa: Adeleorina)—past, present and future. Folia Parasitol 51:99–108. doi: 10.14411/fp.2004.015 CrossRefGoogle Scholar
  22. Farquharson C, Smit NJ, Sikkel PC (2012) Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the eastern Caribbean. Zootaxa 3381:47–61. doi: 10.5281/zenodo.212837 CrossRefGoogle Scholar
  23. Garm A, Watling L (2013) The crustacean integument: setae, setules, and other ornamentation. Funct Morphol Divers 1:167–198CrossRefGoogle Scholar
  24. Graça-Souza AV, Maya-Monteiro C, Paiva-Silva GO, Braz GR, Paes MC, Sorgine MH, Oliveira MF, Oliveira PL (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem Molec 36:322–335. doi: 10.1016/j.ibmb.2006.01.009 CrossRefGoogle Scholar
  25. Green AL, Maypa AP, Almany GR, Rhodes KL, Weeks R, Abesamis RA, Gleason MG, Mumby PJ, White AT (2015) Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biol Rev 90:1215–1247. doi: 10.1111/brv.12155 CrossRefGoogle Scholar
  26. 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. doi: 10.3354/meps115021 CrossRefGoogle Scholar
  27. Grutter AS (1999) Fish cleaning behaviour in Noumea, New Caledonia. Mar Freshw Res 50:209–212. doi: 10.1071/MF97078 CrossRefGoogle Scholar
  28. Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proc R Soc Lond B Biol Sci 268:1361–1365. doi: 10.1098/rspb.2001.1658 CrossRefGoogle Scholar
  29. Grutter AS (2003) Feeding ecology of the fish ectoparasite Gnathia sp. (Crustacea: Isopoda) from the Great Barrier Reef, and its implications for fish cleaning behaviour. Mar Ecol Prog Ser 259:295–302. doi: 10.3354/meps259295 CrossRefGoogle Scholar
  30. Grutter AS, Cribb TH, McCallum H, Pickering JL, McCormick MI (2010) Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis. Coral Reefs 29:31–40. doi: 10.1007/s00338-009-0561-1 CrossRefGoogle Scholar
  31. Grutter AS, Hendrikz J (1999) Diurnal variation in the abundance of juvenile parasitic gnathiid isopods on coral reef fish: implications for parasite–cleaner fish interactions. Coral Reefs 18:187–191. doi: 10.1007/s003380050178 CrossRefGoogle Scholar
  32. Grutter AS, Lester RJ, Greenwood J (2000a) Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods. Mar Ecol Prog Ser 207:123–127. doi: 10.3354/meps207123 CrossRefGoogle Scholar
  33. Grutter AS, Morgan JAT, Adlard RD (2000b) Characterising parasitic gnathiid isopod species and matching life stages with ribosomal DNA ITS2 sequences. Mar Biol 136:201–205. doi: 10.1007/s002270050677 CrossRefGoogle Scholar
  34. Grutter AS, Poulin R (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. doi: 10.3354/meps164263 CrossRefGoogle Scholar
  35. Grutter AS, Rumney JG, Sinclair-Taylor T, Waldie P, Franklin CE (2011) Fish mucous cocoons: the ‘mosquito nets’ of the sea. Biol Lett 7:292–294. doi: 10.1098/rsbl.2010.0916 CrossRefGoogle Scholar
  36. Guégan JF, Hugueny B (1994) A nested parasite species subset pattern in tropical fish: host as major determinant of parasite infracommunity structure. Oecologia 100:184–189. doi: 10.1007/BF00317145 CrossRefGoogle Scholar
  37. Hatcher MJ, Dick JT, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1253–1271. doi: 10.1111/j.1461-0248.2006.00964.x CrossRefGoogle Scholar
  38. Hatcher MJ, Dunn AM (2011) Parasites in ecological communities: from interactions to ecosystems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Heupel MR, Bennett MB (1999) The occurrence, distribution and pathology associated with gnathiid isopod larvae infecting the epaulette shark, Hemiscyllium ocellatum. Int J Parasitol 29:321–330. doi: 10.1016/S0020-7519(98)00218-5 CrossRefGoogle Scholar
  40. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385. doi: 10.1016/j.tree.2006.04.007 CrossRefGoogle Scholar
  41. Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 64:168–176. doi: 10.2307/5752 CrossRefGoogle Scholar
  42. Johnson PT, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371. doi: 10.1016/j.tree.2010.01.005 CrossRefGoogle Scholar
  43. Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864. doi: 10.1111/j.0022-1112.2005.00640.x CrossRefGoogle Scholar
  44. Jones CM, Grutter AS (2007) Variation in emergence of parasitic and predatory isopods among habitats at Lizard Island, Great Barrier Reef. Mar Biol 150:919–927. doi: 10.1007/s00227-006-0416-z CrossRefGoogle Scholar
  45. Justine JL (2010) Parasites of coral reef fish: how much do we know? With a bibliography of fish parasites in New Caledonia. Belgian J Zool 140:155–190Google Scholar
  46. Justine JL, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles JP, Whittington ID (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from snappers and bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquat Biosyst 8:22. doi: 10.1186/2046-9063-8-22 CrossRefGoogle Scholar
  47. Kensley B (1998) Estimates of species diversity of free-living marine isopod crustaceans on coral reefs. Coral Reefs 17:83–88. doi: 10.1007/s003380050100 CrossRefGoogle Scholar
  48. Kramer DL, Chapman MR (1999) Implications of fish home range size and relocation for marine reserve function. Environ Biol Fish 55:65–79. doi: 10.1023/A:1007481206399 CrossRefGoogle Scholar
  49. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518. doi: 10.1038/nature06970 CrossRefGoogle Scholar
  50. Lafferty KD (2013) Parasites in marine food webs. Bull Mar Sci 89:123–134. doi: 10.5343/bms.2011.1124 CrossRefGoogle Scholar
  51. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PT, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546. doi: 10.1111/j.1461-0248.2008.01174.x CrossRefGoogle Scholar
  52. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci 103:11211–11216. doi: 10.1073/pnas.0604755103 CrossRefGoogle Scholar
  53. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513. doi: 10.1016/S0169-5347(02)02615-0 CrossRefGoogle Scholar
  54. Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124:83–99. doi: 10.1017/S003118200200149X CrossRefGoogle Scholar
  55. McKiernan JP, Grutter AS, Davies AJ (2005) Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine. Int J Parasitol 35:19–27. doi: 10.1016/j.ijpara.2004.10.016 CrossRefGoogle Scholar
  56. Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:101–117. doi: 10.1017/S0031182002001476 CrossRefGoogle Scholar
  57. Nagel L, Grutter AS (2007) Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes. J Fish Biol 70:497–508. doi: 10.1111/j.1095-8649.2007.01320.x CrossRefGoogle Scholar
  58. 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 94:569–587. doi: 10.1111/j.1095-8312.2008.00997.x CrossRefGoogle Scholar
  59. Ota Y, Fujita Y, Hirose M (2016) Occurrence of temporary fish ectoparasites (Isopoda; Gnathiidae) in low-salinity subterranean habitats of Miyako-jima Island, Ryukyu Islands, southwestern Japan. Plankton Benthos Res 11:87–95. doi: 10.3800/pbr.11.87 CrossRefGoogle Scholar
  60. Penfold R, Grutter AS, Kuris AM, McCormick MI, Jones CM (2008) Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser 357:111–119. doi: 10.3354/meps07312 CrossRefGoogle Scholar
  61. Poore GC, Bruce NL (2012) Global diversity of marine isopods (except Asellota and crustacean symbionts). PLoS One 7:e43529. doi: 10.1371/journal.pone.0043529 CrossRefGoogle Scholar
  62. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, PrincetonGoogle Scholar
  63. Poulin R, Blasco-Costa I, Randhawa HS (2014) Integrating parasitology and marine ecology: seven challenges towards greater synergy. J Sea Res 113:3–10. doi: 10.1016/j.seares.2014.10.019 CrossRefGoogle Scholar
  64. Quattrini AM, Demopoulos AW (2016) Ectoparasitism on deep-sea fishes in the western North Atlantic: in situ observations from ROV surveys. Int J Parasitol Parasites Wildl 5:217–228. doi: 10.1016/j.ijppaw.2016.07.004 CrossRefGoogle Scholar
  65. Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecol 91:1900–1907. doi: 10.1890/09-1697 CrossRefGoogle Scholar
  66. Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618. doi: 10.1016/j.tree.2008.06.015 CrossRefGoogle Scholar
  67. Ravichandran S, Rameshkumar G, Balasubramanian T (2010) Infestation of isopod parasites in commercial marine fishes. J Parasit Dis 34:97–98. doi: 10.1007/s12639-010-0014-3 CrossRefGoogle Scholar
  68. Roberts CM, Polunin NV (1991) Are marine reserves effective in management of reef fisheries? Rev Fish Biol Fish 1:65–91. doi: 10.1007/BF00042662 CrossRefGoogle Scholar
  69. Rohde K (1976) Species diversity of parasites on the Great Barrier Reef. Parasitol Res 50:93–94Google Scholar
  70. Rowley RJ (1994) Marine reserves in fisheries management. Aquat Conserv 4:233–254. doi: 10.1002/aqc.3270040305 CrossRefGoogle Scholar
  71. Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247. doi: 10.1016/j.anbehav.2003.10.023 CrossRefGoogle Scholar
  72. Sikkel PC, Fuller CA, Hunte W (2000) Habitat/sex differences in time at cleaning stations and ectoparasite loads in a Caribbean reef fish. Mar Ecol Prog Ser 193:191–199. doi: 10.3354/meps193191 CrossRefGoogle Scholar
  73. Sikkel PC, Herzlieb SE, Kramer DL (2005) Compensatory cleaner-seeking behavior following spawning in female yellowtail damselfish. Mar Ecol Prog Ser 296:1–11. doi:  10.3354/meps296001 CrossRefGoogle Scholar
  74. Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689. doi: 10.1007/s00338-006-0154-1 CrossRefGoogle Scholar
  75. Sikkel PC, Sears WT, Weldon B, Tuttle BC (2011) An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod. Mar Biol 158:1075–1083. doi: 10.1007/s00227-011-1631-9 CrossRefGoogle Scholar
  76. 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:e95854. doi: 10.1371/journal.pone.0095854 CrossRefGoogle Scholar
  77. Sikkel PC, Welicky RL, Artim JM, McCammon AM, Sellers JC, Coile AM, Jenkins WG (2016) Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull Mar Sci 93:475–489. doi: 10.5343/bms.2016.1021 CrossRefGoogle Scholar
  78. 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 28:489–495. doi: 10.1007/s00338-009-0474-z CrossRefGoogle Scholar
  79. Smit NJ, Basson L, Van As JG (2003) Life cycle of the temporary fish parasite, Gnathia africana (Crustacea: Isopoda: Gnathiidae). Folia Parasitol 50:135–142. doi: 10.14411/fp.2003.024 CrossRefGoogle Scholar
  80. Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391. doi: 10.1016/S0065-308X(04)58005-3 CrossRefGoogle Scholar
  81. Smit NJ, Grutter AS, Adlard RD, Davies AJ (2006) Hematozoa of teleosts from Lizard Island, Australia, with some comments on their possible mode of transmission and the description of a new hemogregarine species. J Parasitol 92:778–788. doi: 10.1645/GE-756R.1 CrossRefGoogle Scholar
  82. Svavarsson J, Bruce NL (2012) New and little-known gnathiid isopod crustaceans (Cymothoida) from the northern Great Barrier Reef and the Coral Sea. Zootaxa 3380:1–33. doi: 10.5281/zenodo.212640 CrossRefGoogle Scholar
  83. Tanaka K (2007) Life history of gnathiid isopods—current knowledge and future directions. Plankton and Benthos Research 2:1–11. doi: 10.3800/pbr.2.1 CrossRefGoogle Scholar
  84. Tanaka K, Aoki M (1998) Crustacean infauna of the demosponge Halichondria okadai (Kadota) with reference to the life cycle of Gnathia sp. (Isopoda: Gnathiidea). In: Watanabe Y, Fusetani N (eds) Sponge science: multidisciplinary perspectives. Springer-Verlag, Tokyo, pp 259–267Google Scholar
  85. Tanaka K, Nishi E (2008) Habitat use by the gnathiid isopod Elaphognathia discolor living in terebellid polychaete tubes. J Mar Biol Assoc UK 88:57–63. doi: 10.1017/S0025315408000039 CrossRefGoogle Scholar
  86. Thomas F, Renaud F, de Meeûs T, Poulin R (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proc R Soc Lond B Biol Sci 265:1091–1096. doi: 10.1098/rspb.1998.0403 CrossRefGoogle Scholar
  87. Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85. doi: 10.1111/j.1365-2656.2004.00899.x CrossRefGoogle Scholar
  88. Triki Z, Grutter AS, Bshary R, Ros AF (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163:187. doi: 10.1007/s00227-016-2959-y CrossRefGoogle Scholar
  89. Welicky RL, Cheney KL, Coile AM, McCammon A, Sikkel PC (2013) The relationship between lunar periodicity and activity of fish-parasitic gnathiid isopods in the Caribbean. Mar Biol 160:1607–1617. doi: 10.1007/s00227-013-2213-9 CrossRefGoogle Scholar
  90. Whiteman EA, Côté IM (2002) Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons. J Fish Biol 60:1443–1458. doi: 10.1111/j.1095-8649.2002.tb02439.x CrossRefGoogle Scholar
  91. Williams JD, Madad AZ (2010) A new species and record of branchial parasitic isopods (Crustacea: Isopoda: Bopyridae: Pseudioninae) of porcellanid crabs from the Philippines. Exp Parasitol 125:23–29. doi: 10.1016/j.exppara.2009.09.012 CrossRefGoogle Scholar
  92. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AM (2007) Parasites alter community structure. Proc Natl Acad Sci 104:9335–9339. doi: 10.1073/pnas.0700062104 CrossRefGoogle Scholar
  93. Wood CL, Lafferty KD (2015) How have fisheries affected parasite communities? Parasitology 142:134–144. doi: 10.1017/S003118201400002X CrossRefGoogle Scholar
  94. Wood CL, Lafferty KD, Micheli F (2010) Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol Lett 13:761–775. doi: 10.1111/j.1461-0248.2010.01467.x CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institute of Environmental and Marine SciencesSilliman UniversityDumaguete CityPhilippines
  2. 2.Department of Biological Sciences and Environmental Sciences ProgramArkansas State UniversityJonesboroUSA
  3. 3.Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom CampusNorth-West UniversityPotchefstroomSouth Africa

Personalised recommendations