Skip to main content
SpringerLink
Log in

The Ecological Significance of Parasitic Crustaceans

  • Chapter
  • First Online:
Book cover Parasitic Crustacea

Part of the book series: Zoological Monographs ((ZM,volume 3))

Abstract

Despite that aquatic parasite diversity and abundance likely surpasses that of terrestrial parasites, our understanding of aquatic parasites lags far behind our knowledge of terrestrial parasites. This is undoubtedly attributable to our being terrestrial primates and the associated logistical challenges of studying most aquatic environments. However, with improving technology that allows for more extended exploration of aquatic environments and the continued maturation of host-parasite ecology and functional biodiversity as fields of inquiry, our understanding of parasitic crustaceans is rapidly extending beyond identification and description of life cycles to describing the role of parasites in ecosystems. Both field and laboratory studies have demonstrated that parasitic organisms play critical roles at the individual, population and community levels. In this chapter, we explore these roles for parasitic isopods and copepods in particular and highlight recent studies that employ current methodologies in ecological research such as molecular and stable isotope analyses. This chapter should demonstrate to readers that there are still far more questions than answers about the role of parasitic Crustacea in aquatic systems, but based on what we know today, we can say they are likely one of the most critical players in aquatic ecosystem dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe T, Sekiguchi K, Onishi H, Muramatsu K, Kamito T (2012) Observations on a school of ocean sunfish and evidence for a symbiotic cleaning association with albatrosses. Mar Biol 159:1173–1176

    Article  Google Scholar 

  • Adlard RD, Lester RJG (1994) Dynamics of the interaction between the parasitic isopod, Anilocra pomacentri, and the coral reef fish, Chromis nitida. Parasitology 109:311–324

    Article  PubMed  Google Scholar 

  • Adlard RD, Miller TL, Smit NJ (2015) The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitol 31(4):160–166

    Article  PubMed  Google Scholar 

  • Albright R, Langdon C (2011) Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob Change Biol 17:2478–2487

    Article  Google Scholar 

  • Amanieu M (1963) Evolution des populations de Paragnathia formica (Hesse) au cours d’un cycle annuel. Bull Inst Océanogr, Monaco 60:1–12

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Aneesh P-T, Sudha K, Arshad K, Anilkumar G, Trilles J-P (2013) Seasonal fluctuation of the prevalence of cymothoids representing the genus Nerocila (Crustacea, Isopoda), parasitizing commercially exploited marine fishes from the Malabar Coast, India. Acta Parasitologica 58:80–90

    Article  PubMed  Google Scholar 

  • Arias-González JE, Morand S (2006) Trophic functioning with parasites: a new insight for ecosystem analysis. Mar Ecol Prog Ser 320:43–53

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Arnal C, Morand S (2001) Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus. Mar Biol 138:777–784

    Article  Google Scholar 

  • Artim JM, Sikkel PC (2013) Live coral repels a common reef-fish ectoparasite. Coral Reefs 32:487–494

    Article  Google Scholar 

  • Artim JM, Sikkel PC (2016) Comparison of sampling methodologies and estimation of population parametres for a temporary fish ectoparasite. Int J Parasitol Parasites Wildl 5:145–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Artim JM, Hook A, Grippo RS, Sikkel PC (2017) Predation on parasitic gnathiid isopods on coral reefs: a comparison of Caribbean cleaning gobies with non-cleaning microcarnivores. Coral Reefs 36(4):1213–1223

    Article  Google Scholar 

  • Athanassopoulou FD, Bouboulis B, Martinsen B (2001) In vitro treatments of deltamethrin against the isopod parasite Anylocra physodes, a pathogen of sea bass Dicentrarchus labrax. L. Bull Eur Assoc Fish Pathol 21:26–29

    Google Scholar 

  • Beaugrand G, Reid PC, Ibañez F, Planque B (2000) Biodiversity of North Atlantic and North Sea caanoid copepods. Mar Ecol Prog Ser 204:299–303

    Article  Google Scholar 

  • Becker JHA, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515–520

    Google Scholar 

  • Behrens JW, Seth H, Axelsson M, Buchmann K (2014) The parasitic copepod Lernaeocera branchialis negatively affects cardiorespiratory function in Gadus morhua. J Fish Biol 84:1599–1606

    Article  CAS  PubMed  Google Scholar 

  • Bergeron DH, Perkins PJ (2014) Evaluating the usefulness of three indices for assessing winter tick abundance in northern New Hampshire. Alces 50:1–15

    Google Scholar 

  • Binning SA, Roche DG, Layton C (2013) Ectoparasites increase swimming costs in a coral reef fish. Biol Lett 9:20120927

    Article  PubMed  PubMed Central  Google Scholar 

  • Binning SA, Barnes JI, Davies JN, Backwell PRY, Keogh JS, Roche DG (2014) Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Anim Behav 93:1–7

    Article  Google Scholar 

  • Binning SA, Roche DG, Grutter AS, Colosio S, Sun D, Miest J, Bshary R (2018) Cleaner wrasse indirectly affect the cognitive performance of a damselfish through ectoparasite removal. Proc R Soc B 285:20172447

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Blakeslee AMH, Fowler AE, Keogh CL (2013) Marine invasions and parasite escape: updates and new perspectives. In: Lesser MP (ed) Advances in marine biology, 1st edn. Academic Press, Cambridge, pp 87–169

    Google Scholar 

  • Blasco-Costa I, Rouco C, Pouli R (2015) Biogeography of parasitism in freshwater fish: spatial patterns in hot spots of infection. Ecography 38:301–310

    Article  Google Scholar 

  • Boag B, Neilson R, Robinson D, Scrimgeour CM, Handley LL (1998) Wild rabbit host and some parasites show trophic–level relationships for δ13C and δ15N: a first report. Isotope Environ Health Stud 34:81–85

    Article  CAS  Google Scholar 

  • Bonaldo RM, Grutter AS, Sazima I, Krajewski JP (2015) 24/7 service: nocturnal cleaning in a tropical Indo-Pacific reef. Mar Biodivers 45(4):611–612

    Article  Google Scholar 

  • Bowman TE (1960) Description and notes on the biology of Lironeca puhi, n. sp. (Isopoda: Cymothoidae), parasite of the Hawaiian moray eel Gymnothorax eurostus (Abbott). Crustaceana 1:84–91

    Article  Google Scholar 

  • Boxshall GA (1974) The population dynamics of Lepeophtheirus pectoralis (Müller): seasonal variation in abundance and age structure. Parasitology 69:361–371

    Article  CAS  PubMed  Google Scholar 

  • Boxshall G (2005) Crustacean parasites. In: Rohde K (ed) Marine parasitology. CSIRO Publishing, Clayton, pp 123–169

    Google Scholar 

  • Brønseth T, Folstad I (1997) The effect of parasites on courtship dance in threespine stickle-backs: more than meets the eye? Can J Zool 75:589–594

    Article  Google Scholar 

  • Brooker AJ, Shinn AP, Bron JE (2007) A review of the biology of the parasitic copepod Lernaeocera branchialis (L., 1767) (Copepoda: Pennellidae). Adv Parasitol 65:297–341

    Article  PubMed  Google Scholar 

  • Brooks KM (2005) The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Rev Fish Sci 13(3):177–204

    Article  Google Scholar 

  • Brooks DR, Hoberg EP (2007) How will global climate change affect parasite–host assemblages? Trends Parasitol 23(12):571–574

    Article  PubMed  Google Scholar 

  • Bruce NL (1987a) Australian Pleopodias Richardson, 1910 and Anilocra Leach, 1818 (Isopoda: Cymothoidae), crustacean parasites of marinefishes. Rec Aust Mus 39:85–130

    Article  Google Scholar 

  • Bruce NL (1987b) Australian Renocila Miers, 1880 (Isopoda: Cymothoidae), crustacean parasites of marine fishes. Rec Aust Mus 39:169–182

    Article  Google Scholar 

  • Brusca RC (1978) Studies on the cymothoid fish symbionts of the eastern Pacific (Isopoda, Cymothoidae) I. Biology of Nerocila californica. Crustaceana 34:141–154

    Article  Google Scholar 

  • Budge SM, Wooller MJ, Springer AM, Iverson SJ, McRoy CP, Divoky GJ (2008) Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 157:117–129

    Article  CAS  PubMed  Google Scholar 

  • Bunkley-Williams L, Williams EH (1998a) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–896

    Article  CAS  PubMed  Google Scholar 

  • Bunkley-Williams L, Williams EH (1998b) Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana 71:862–869

    Article  Google Scholar 

  • Byers JE (2009) Including parasites in food webs. Trends Parasitol 25:55–57

    Article  PubMed  Google Scholar 

  • Cacabelos E, Olabarria C, Incera M (2010) Effects of habitat structure and tidal height on epifaunal assemblages associated with macroalgae. Estuaries Coast Shelf Sci 89:43e52

    Google Scholar 

  • Cantrell CE, Henry RP, Chadwick NE (2015) Nitrogen transfer in a Caribbean mutualistic network. Mar Biol 162:1–12

    Article  CAS  Google Scholar 

  • Carr MH, Hixon MA (1995) Predation effects on early post-settlement survivorship of coral-reef fishes. Mar Ecol Prog Ser 124:31–42

    Article  Google Scholar 

  • Chambers SD, Sikkel PC (2002) Diel emergence patterns of ecologically important, fish parasitic, Gnathiid isopod larvae on Caribbean coral reefs. Caribb J Sci 38:37–43

    Google Scholar 

  • Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165

    Article  PubMed  PubMed Central  Google Scholar 

  • Chew LL, Chong VC, Ooi AL, Sasekumar A (2015) Vertical migration and positioning behavior of copepods in a mangrove estuary: interactions between tidal, diel light and lunar cycles. Estuaries Coast Shelf Sci 152:142–152

    Article  Google Scholar 

  • Cizauskas CA, Carlson CJ, Burgio KR, Clements CF, Dougherty ER, Harris NC, Phillips AJ (2017) Parasite vulnerability to climate change: an evidence-based functional trait approach. Roy Soc Open Sci 4:160535

    Article  Google Scholar 

  • Clague GE, Cheney KL, Goldzien AW, McCormick MI, Waldie PA, Grutter AS (2011) Long-term cleaner fish presence affects growth of a coral reef fish. Biol Lett 7:863–865

    Article  PubMed  PubMed Central  Google Scholar 

  • Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock T, Parker G (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  • Cocheret De La Morinière E, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove–seagrass–reef continuum: stable isotope and gut content analysis. Mar Ecol Prog Ser 246:279–289

    Article  Google Scholar 

  • Coetzee ML, Smit NJ, Grutter AS, Davies AJ (2009) Gnathia trimaculata n. sp. (Crustacea: Isopoda: Gnathiidae), an ectoparasite found parasitising requiem sharks from off Lizard Island, Great Barrier Reef, Australia. Syst Parasitol 72:97–112

    Article  PubMed  Google Scholar 

  • Cohen BF, Poore GC (1994) Phylogeny and biogeography of the Gnathiidae (Crustacea: Isopoda) with descriptions of new genera and species, most from south-eastern Australia. Mem Mus Victoria 54:271–397

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 113:3875–3880

    Article  CAS  PubMed  Google Scholar 

  • Connors BM, Krkosek M, Dill LM (2008) Sea lice escape predation on their host. Biol Lett 4:455–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connors BM, Lagasse C, Dill LM (2011) What’s love got to do with it? Ontogenetic changes in drivers of dispersal in a marine ectoparasite. Behav Ecol 22:588–593

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Costello MJ (2006) Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol 22(10):475–483

    Article  PubMed  Google Scholar 

  • Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Mar Bio Oceanogr Ann Rev 38:311–355

    Google Scholar 

  • Côté IM, Molloy PP (2003) Temporal variation in cleanerfish and client behaviour: does it reflect ectoparasite availability? Ethology 109:487–499

    Article  Google Scholar 

  • Côté IM, Soares MC (2011) Gobies as cleaners. In: Patzner RA, Van Tassel JL, Kovacic M, Kapoor BG (eds) The biology of gobies. Science, Jersey, pp 531–558

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Davies AJ (1982) Further studies on Haemogregarina bigemina Laveran & Mesnil, the marine fish Blennius pholis, L. and the isopod Gnathia maxillaris. J Protozool 29:576–583

    Article  Google Scholar 

  • Davies AJ (1995) The biology of fish haemogregarines. Adv Parasitol 36:118–203

    Google Scholar 

  • 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 

  • Davies AJ, Eiras JC, Austin RTE (1994) Investigations into the transmission of Haemogregarina bigemina Laveran & Mesnil, 1901 (Apicomplexa: Adeleorina) between intertidal fishes in Portugal. J Fish Dis 17:283–289

    Article  Google Scholar 

  • Davies AJ, Curtis L, Grutter AS, Smit NJ (2009) Suspected viral erythrocytic necrosis (VEN) in a blackbar triggerfish, Rhinecanthus aculeatus, from Lizard Island, Great Barrier Reef, Australia. Mar Biodivers Rec 2:1–4

    Article  Google Scholar 

  • De Troch M, Boeckx P, Cnudde C, Van Gansbeke D, Vanreusel A, Vincx M, Caramujo MJ (2012) Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67

    Article  CAS  Google Scholar 

  • Demopoulos AW, Sikkel PC (2015) Enhanced understanding of ectoparasite–host trophic linkages on coral reefs through stable isotope analysis. Int J Parasitol Parasites Wildl 4:125–134

    Article  PubMed  PubMed Central  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Deudero S, Pinnegar JK, Polunin NVC (2002) Insights into fish host–parasite trophic relation-ships revealed by stable isotope analysis. Dis Aquat Org 52:77–86

    Article  Google Scholar 

  • Doi H, Yurlova NI, Vodyanitskaya SN, Kanaya G, Shikano S, Kikuchi E (2010) Estimating isotope fractionation between cercariae and host snail with the use of isotope measurement designed for very small organisms. J Parasitol 96:314–317

    Article  PubMed  Google Scholar 

  • Doucett RR, Booth RK, Power G, McKinley RS (1999) Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable–isotope analysis. Can J Fish Aquat Sci 56:2172–2180

    Article  Google Scholar 

  • Dunlap DS, Ng TF, Rosario K, Barbosa JG, Greco AM, Breitbart M, Hewson I (2013) Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci 110(4):1375–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM et al (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biol 11:e1001579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Escribano R, Hidalgo P (2000) Spatial distribution of copepods in the north of the Humboldt Current region off Chile during coastal upwelling. J Mar Biol Assoc UK 80:283–290

    Article  Google Scholar 

  • Farquharson C, Smit NJ, Sikkel PC (2012) Description of a new species of gnathiid (Crustacea, Isopoda, Gnathiidae) from the Caribbean. Zootaxa 3381:47–61

    Article  Google Scholar 

  • 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 95:1066–1075

    Article  PubMed  Google Scholar 

  • 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 

  • Fitze PS, Tschirren B, Richner H (2004) Life history and fitness consequences of ectoparasites. J Anim Ecol 73:216–226

    Article  Google Scholar 

  • Flamarique IN, Browman HI, Belanger M, Boxaspen K (2000) Ontogenetic changes in visual sensitivity of the parasitic salmon louse Lepeophtheirus salmonis. J Exp Biol 203:649–1657

    Google Scholar 

  • Floeter SR, Vazquez DP, Grutter AS (2007) The macroecology of marine cleaning mutualisms. J Anim Ecol 76:105–111

    Article  PubMed  Google Scholar 

  • Fogelman RM, Grutter AS (2008) Mancae of the parasitic cymothoid isopod, Anilocra apogonae: early life history, host-specificity, and effect on growth and survival of preferred young cardinal fishes. Coral Reefs 27:685–693

    Article  Google Scholar 

  • Fogelman RM, Kuris AM, Grutter AS (2009) Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five–lined cardinalfish, Cheilodipterus quinquelinatus. Int J Parasitol 39:577–583

    Article  PubMed  Google Scholar 

  • Folstad I, Hope AM, Karter A, Skorping A (1994) Sexually selected color in male Sticklebacks – a signal of both parasite exposure and parasite resistance. Oikos 69:511–515

    Article  Google Scholar 

  • Forrester GE, Finley RJ (2006) Parasitism and a shortage of refuges jointly mediate the strength of density dependence in a reef fish. Ecology 87:1110–1115

    Article  PubMed  Google Scholar 

  • Frazer LN (2009) Sea-cage aquaculture, sea lice, and declines of wild fish. Conserv Biol 23(3):599–607

    Article  PubMed  Google Scholar 

  • Gaard E, Gislason A, Falkenhau T, Søiland H, Musaeva E, Vereshchaka A, Vinogradov G (2008) Horizontal and vertical copepod distribution and abundance on the Mid-Atlantic Ridge in June 2004. Deep Sea Res Part II Topical Stud Oceanogr 55:59–71

    Article  Google Scholar 

  • Galil BS (2000) A sea under siege–alien species in the Mediterranean. Biol Invasions 2:177–186

    Article  Google Scholar 

  • Giorgi MS, Arlettaz R, Guillaume F, Nussle S, Ossola C, Vogel P, Christie P (2004) Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138:648–654

    Article  PubMed  Google Scholar 

  • Gomez-Diaz E, Gonzalez-Solis J (2010) Trophic structure in a seabird host–parasite food web: insights from stable isotope analyses. PLoS One 5:533546

    Article  CAS  Google Scholar 

  • Gorlick DL, Atkins PD, Losey GS (1978) Cleaning stations as water holes, garbage dumps, and sites for evolution of reciprocal altruism. Am Nat 112:341–353

    Article  Google Scholar 

  • Gorlick D, Atkins P, Losey G (1987) Effect of cleaning by Labroides dimidiatus (Labridae) on an ectoparasite population infecting Pomacentrus vaiuli (Pomacentridae) at Enewetak Atoll. Copeia 1987:41–45

    Article  Google Scholar 

  • 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 Mol Biol 36:322–335

    Article  PubMed  CAS  Google Scholar 

  • Green SJ, Côté IM (2014) Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities. J Anim Ecol 83:1451–1460

    Article  PubMed  Google Scholar 

  • Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Grutter AS (1997a) Spatio-temporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997:46–355

    Article  Google Scholar 

  • Grutter AS (1997b) Size-selective predation by the cleaner fish Labroides dimidiatus. J Fish Biol 50:1303–1308

    Google Scholar 

  • Grutter AS (1999) Infestation dynamics of gnathiid isopod juveniles parasitic on the coral-reef fish Hemigymnus melapterus (Labridae). Mar Biol 61:545–552

    Article  Google Scholar 

  • Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proc R Soc Lond 268:1361–1365

    Article  CAS  Google Scholar 

  • Grutter AS (2002) Cleaning symbioses from the parasites’ perspective. Parasitology 124:65–81

    Article  Google Scholar 

  • Grutter AS, Feeney WE (2016) Equivalent cleaning in a juvenile facultative and obligate cleaning wrasse: an insight into the evolution of cleaning in labrids? Coral Reefs 35(3):991–997

    Article  Google Scholar 

  • Grutter AS, Pankhurst NW (2000) The effects of capture, handling, confinement and ectoparasite load on plasma levels of cortisol, glucose and lactate in the coral reef fish Hemigymnus melapterus. J Fish Biol 57:391–401

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Grutter AS, Lester RJG, Greenwood J (2000) Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods. Mar Ecol Prog Ser 207:123–127

    Article  Google Scholar 

  • Grutter AS, Murphy J, Choat H (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67

    Article  CAS  PubMed  Google Scholar 

  • Grutter AS, Pickering JL, McCallum H, McCormick MI (2008) Impact of micropredatory gnathiid isopods on young coral reef fishes. Coral Reefs 27:655–661

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Grutter AS, Blomberg SP, Fargher B, Kuris AM, McCormick MI, Warner RR (2017) Size-related mortality due to gnathiid isopod micropredation correlates with settlement size in coral reef fishes. Coral Reefs 36:549–559

    Article  Google Scholar 

  • Grutter AS, De Brauwer M, Bshary R, Cheney KL, Cribb TH, Madin EMP, McClure EC, Meekan MG, Sun D, Warner RR, Werminghausen J, Sikkel PC (2018) Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37:15–24

    Article  Google Scholar 

  • Guimarães PR, Sazima C, Reis SF, Sazima I (2007) The nested structure of marine cleaning symbiosis: is it like flowers and bees? Biol Lett 3:51–54

    Article  PubMed  Google Scholar 

  • Hadfield KA, Bruce NL, Smit NJ (2013) Review of the fish–parasitic genus Cymothoa Fabricius, 1783 (Isopoda, Cymothoidae, Crustacea) from the south-western Indian Ocean, including a new species from South Africa. Zootaxa 3640:152–176

    Article  PubMed  Google Scholar 

  • Hadfield KA, Bruce NL, Smit NJ (2014) Review of the fish parasitic genus Ceratothoa Dana, 1852 (Crustacea, Isopoda, Cymothoidae) from South Africa, including the description of two new species. ZooKeys 400:1–42

    Article  Google Scholar 

  • Hadfield KA, Bruce NL, Smit NJ (2015) Review of Mothocya Costa, in Hope, 1851 (Crustacea: Isopoda: Cymothoidae) from southern Africa, with the description of a new species. Afr Zool 50:147–163

    Article  Google Scholar 

  • Hadfield KA, Bruce NL, Smit NJ (2016) Redescription of poorly known species of Ceratothoa Dana, 1852 (Crustacea, Isopoda, Cymothoidae), based on original type material. ZooKeys 592:39–91

    Article  Google Scholar 

  • Hall ER, Vaughan D, Crosby MP (2012) Development of ocean acidification flow-thru experimental raceway units (OAFTERU). In: Proceedings of the 12th international coral reef symposium 34236:9–13

    Google Scholar 

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

    Book  Google Scholar 

  • 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 Gnathia aureamaculosa Ferreira & Smit, isopods. J Fish Dis 34:563–566

    Article  CAS  PubMed  Google Scholar 

  • Heagney EC, Gillanders BM, Suthers IM (2013) The effect of parasitism by a blood-feeding isopod on the otolith chemistry of host fish. Mar Freshw Res 64:10–19

    Article  CAS  Google Scholar 

  • Heckmann R (2003) Other ectoparasites infesting fish: Copepods, branchiurans, isopods, mites and bivalves. Aquac Mag Ark 29:20–31

    Google Scholar 

  • Heuch PA, Parsons A, Boxaspen K (1995) Diel vertical migration: a possible host–finding mechanism in salmon louse (Lepeophtheirus salmonis) copepodids? Can J Fish Aquat Sci 52:681–689

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hevrøy EM, Boxaspen K, Oppedal F, Taranger GL, Holm JC (2003) The effect of artificial light treatment and depth on the infestation of the sea louse Lepeophtheirus salmonis on Atlantic salmon (Salmo salar L.) culture. Aquaculture 220:1–14

    Article  Google Scholar 

  • Hixon MA (2015) Predation: piscivory and the ecology of coral–reef fishes. In: Mora C (ed) Ecology of fishes on coral reefs. Cambridge University Press, Cambridge, pp 41–54

    Chapter  Google Scholar 

  • Hobson ES (1971) Cleaning symbiosis among California inshore fishes. Fish Bull 69:491–524

    Google Scholar 

  • Holdich DM, Harrison K (1980) The crustacean isopod genus Gnathia Leach from Queensland waters with descriptions of nine new species. J Mar Freshw Res 31:215–240

    Article  Google Scholar 

  • Honma Y, Chiba A (1991) Pathological changes in the branchial chamber wall of stingrays, Dasyatis spp., associated with the presence of juvenile gnathiids (Isopoda, Crustacea). Fish Pathol 26:9–16

    Article  Google Scholar 

  • 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 26:401–406

    Article  CAS  PubMed  Google Scholar 

  • Hsieh CHH, Chiu TS, Shih CT (2004) Copepod diversity and composition as indicators of intrusion of the Kuroshio Branch Current into the Northern Taiwan Strait in spring 2000. Zool Stud 43:393–403

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Huebner LK, Chadwick NE (2012a) Patterns of cleaning behaviour on coral reef fish by the anemoneshrimp Ancylomenes pedersoni. J Mar Biol Assoc UK 92:1557–1562

    Article  Google Scholar 

  • Huebner LK, Chadwick NE (2012b) Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp. J Exp Mar Biol Ecol 417:237–242

    Article  Google Scholar 

  • Iken K, Brey T, Wand U, Voigt J, Junghans P (2001) Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog Oceanogr 50:383–405

    Article  Google Scholar 

  • Incze LS, Hebert D, Wolff N, Oakey N, Dye D (2001) Changes in copepod distributions associated with increased turbulence from wind stress. Mar Ecol Prog Ser 213:229–240

    Article  Google Scholar 

  • Jacoby CA, Greenwood JG (1988) Spatial, temporal, and behavioral patterns in emergence of zooplankton in the lagoon of Heron Reef, Great Barrier Reef, Australia. Mar Biol 97:309–328

    Article  Google Scholar 

  • Jenkins WG, Demopoulos AWJ, Sikkel PC (2018a) Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods. Symbiosis 75:113–121

    Article  Google Scholar 

  • Jenkins WG, Demopoulos AW, Sikkel PC (2018b) Host feeding ecology and trophic position significantly influence isotopic discrimination between a generalist ectoparasite and its hosts: Implications for parasite-host trophic studies. Food Webs 16:e00092

    Article  Google Scholar 

  • Johannesen A (1978) Early stages of Lepeophtheirus salmonis (Copepoda: Caligidae). Sarsia 63:169–176

    Article  Google Scholar 

  • Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z (2004) A review of the impact of parasitic copepods on marine aquaculture. Zool Stud 43:229–243

    Google Scholar 

  • Johnson PTJ, 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

    Article  PubMed  Google Scholar 

  • Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive Hemigymnus melapterus (Bloch) (Pisces: Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jones CM, Grutter AS (2008) Reef-based micropredators reduce the growth of post-settlement damselfish in captivity. Coral Reefs 27:677–684

    Article  Google Scholar 

  • Jones SR, Hargreaves NB (2007) The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon in coastal British Columbia. J Parasitol 93:1324–1331

    Article  PubMed  Google Scholar 

  • Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37:927–935

    Article  CAS  PubMed  Google Scholar 

  • Jones CM, Miller TL, Grutter AS, Cribb TH (2008) Natatory–stage cymothoid isopods: description, molecular identification and evolution of attachment. Int J Parasitol 38:477–491

    Article  CAS  PubMed  Google Scholar 

  • Jormalainen V, Honkanen T, Makinen A, Hemmi A, Vesakoski O (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea baltica. Oikos 93:77–86

    Article  Google Scholar 

  • Kabata Z, Cousens B (1977) Host–parasite relationships between sockeye salmon, Oncorhynchus nerka, and Salmincola californiensis (Copepoda: Lernaeopodidae). J Fish Board Can 34:191–202

    Article  Google Scholar 

  • Kensley B (1998) Estimates of species diversity of free-living marine isopod crustaceans on coral reefs. Coral Reefs 17:83–88

    Article  Google Scholar 

  • Khokhlova IS, Serobyan V, Degen AA, Krasnov BR (2010) Host gender and offspring quality in a flea parasitic on a rodent. J Exp Biol 213:3299–3304

    Article  PubMed  Google Scholar 

  • Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2004) Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. Am Nat 164:506–516

    PubMed  Google Scholar 

  • Krkošek M, Revie CW, Gargan PG, Skilbrei OT, Finstad B, Todd CD (2013) Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean. Proc R Soc B Biol Sci 280:20122359

    Article  Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP et al (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanog 44:925–931

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Mercedes P, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546

    Article  PubMed  PubMed Central  Google Scholar 

  • Leray M, Knowlton N (2014) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc Natl Acad Sci 112:2076–2081

    Article  CAS  Google Scholar 

  • Limbaugh C (1961) Cleaning symbiosis. Sci Am 205:42–49

    Article  Google Scholar 

  • Loot G, Poulet N, Reyjol Y, Blanchet S, Lek S (2004) The effects of the ectoparasite Tracheliastes polycolpus (Copepoda: Lernaeopodidae) on the fins of rostrum dace (Leuciscus leuciscus bur-digalensis). Parasitol Res 94:16–23

    Article  PubMed  Google Scholar 

  • Losey GS (1972) Ecological importance of cleaning symbiosis. Copeia 1972:820–833

    Article  Google Scholar 

  • Losey GS (1974) Cleaning symbiosis in Puerto Rico with comparison to the tropical Pacific. Copeia 1974:960–970

    Article  Google Scholar 

  • Mackas DL, Sefton H, Miller CB, Raich A (1993) Vertical habitat partitioning by large calanoid copepods in the oceanic subarctic Pacific during spring. Prog Oceanogr 32:259–294

    Article  Google Scholar 

  • Mackenzie K (1999) Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Poll Bull 38:955–959

    Article  CAS  Google Scholar 

  • Manship BM, Walker AJ, Jones LA, Davies AJ (2011) Blood feeding in juvenile Paragnathia formica (Isopoda: Gnathiidae): biochemical characterization of trypsin inhibitors, detection of antico-agulants, and molecular identification of fish hosts. Parasitology 139:744–754

    Article  CAS  Google Scholar 

  • Maran BA, Moon SY, Ohtsuka S, Oh SY, Soh H-Y, Myoung J-G, Iglikowska A, Boxshall GA (2013) The caligid life cycle: new evidence from Lepeophtheirus elegans reconciles the cycles of Caligus and Lepeophtheirus (Copepoda: Caligidae). Parasite 20:1–15

    Article  Google Scholar 

  • Marcogliese DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Can J Zool 79(8):1331–1352

    Article  Google Scholar 

  • Marcogliese DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev Sci Tech 27(2):467–484

    Article  CAS  PubMed  Google Scholar 

  • Marcogliese D, Cone D (1997) Food webs: a plea for parasites. Trends Ecol Evol 12:320–325

    Article  CAS  PubMed  Google Scholar 

  • Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545

    Article  PubMed  Google Scholar 

  • McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Meadows DW, Meadows CM (2003) Behavioral and ecological correlates of foureye butterflyfish, Chaetodon capistratus, (Perciformes: Chaetodontidae) infected with Anilocra chaetodontis (Isopoda: Cymothoidae). Rev Biol Trop 51(Suppl 4):77–81

    PubMed  Google Scholar 

  • Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecol Lett 13:838–848

    Article  PubMed  Google Scholar 

  • Meyer JL, Schultz ET (1985) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156

    Article  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Monod T (1926) Les Gnathiidae. Essai Monographique (Morphologie, Biologie, Systématique). Mémoires de la Société Royale des Sciences naturelles du Maroc 13:1–668

    Google Scholar 

  • Morand S, Arias González E (1997) Is parasitism a missing ingredient in model ecosystems? Ecol Model 95:61–74

    Article  Google Scholar 

  • Mordue AJ, Birkett MA (2009) A review of host finding behaviour in the parasitic sea louse, Lepeophtheirus salmonis (Caligidae: Copepoda). J Fish Dis 32:3–13

    Article  Google Scholar 

  • Mugridge RER, Stallybrass HG (1983) A mortality of eels, Anguilla anguilla L., attributed to Gnathiidae. J Fish Biol 6:81–82

    Google Scholar 

  • Nagasawa K (2001) Annual changes in the population size of the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) on high–seas Pacific salmon (Oncorhynchus spp.), and relationship to host abundance. Hydrobiologia 453:411–416

    Article  Google Scholar 

  • Nagasawa K, Ishida Y, Ogura M, Tadokoro K, Hiramatsu K (1993) The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on six species of Pacific salmon in offshore waters of the North Pacific Ocean and Bering Sea. Pathog Wild Farmed Fish Sea Lice 1:166–178

    Google Scholar 

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

    Article  Google Scholar 

  • Nagel L, Montgomerie R, Lougheed S (2008) Evolutionary divergence in common marine ec-toparasites Gnathia spp. (Isopoda: Gnathiidae) on the Great Barrier Reef: phylogeography, morphology, and behaviour. Biol J Linnean Soc 94:569–587

    Article  Google Scholar 

  • Narvaez P, Barreiros JP, Soares MC (2015) The parasitic isopod Anilocra physodes, as a novel food source for the lizardfish Synodus saurus (Synodontidae). Cybium 39:313–314

    Google Scholar 

  • Neilson R, Boag B, Hartley G (2005) Temporal host–parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses. Parasitology 131:279–285

    Article  CAS  PubMed  Google Scholar 

  • Nie P, Yao WJ (2000) Seasonal population dynamics of parasitic copepods, Sinergasilus spp. on farmed fish in China. Aquacult 187:239–245

    Article  Google Scholar 

  • O’Grady SP, Dearing MD (2006) Isotopic insight into host–endosymbiont relationships in Liolaemid lizards. Oecologia 150:355–361

    Article  PubMed  Google Scholar 

  • Oldewage WH (1992) Occurrence and distribution of parasitic Copepoda (Crustacea) off the southern coast of South Africa. S Afr J Wildl Res 22:33–35

    Google Scholar 

  • Östlund-Nilsson S, Curtis L, Nilsson GE, Grutter AS (2005) Parasitic isopod Anilocra apogonae, a drag for the cardinal fish Cheilodipterus quinquelineatus. Mar Ecol Prog Ser 287:209–216

    Article  Google Scholar 

  • 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 159:2333–2347

    Article  CAS  Google Scholar 

  • Palacios-Fuentes P, Landaeta MF, Muñoz G, Plaza G, Ojeda FP (2012) The effects of a parasitic copepod on the recent larval growth of a fish inhabiting rocky coasts. Parasitol Res 111:1661–1671

    Article  PubMed  Google Scholar 

  • Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102

    Article  Google Scholar 

  • Paperna I, Por FD (1977) Preliminary data on the Gnathiidae (Isopoda) of the Northern Red Sea, the Bitter Lakes, and the Mediterranean and the biology of Gnathia piscivora n. sp. Rapports et Proces–Verbaux des Reunions–Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranée (CIESM) 24:195–197

    Google Scholar 

  • Parker D, Booth AJ (2013) The tongue-replacing isopod Cymothoa borbonica reduces the growth of largespot pompano Trachinotus botla. Mar Biol 160(11):2943–2950

    Article  Google Scholar 

  • Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alternative acanthocephalan infections in native fish. J Anim Ecol 80:990–998

    Article  PubMed  Google Scholar 

  • Penfold R, Grutter AS, Kuris AM, McCormick M, Jones CM (2008) Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser 357:111–119

    Article  Google Scholar 

  • Petchey OL, Beckerman AP, Riede JO, Warren PH (2008) Size, foraging, and food web structure. Proc Natl Acad Sci 105:4191–4196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen CW (1995) Male mating success and female choice in permanently territorial damselfishes. Bull Mar Sci 57:690–704

    Google Scholar 

  • Pimm SL (2002) Food webs. The University of Chicago Press, Chicago

    Google Scholar 

  • Pinnegar J, Campbell N, Polunin NVC (2001) Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships. J Fish Biol 59:494–503

    Google Scholar 

  • Pino-Marambio J, Mordue Luntz AJ, Birkett M, Carvajal J, Asencio G, Mellado A, Quiroz A (2007) Behavioural studies of host, non-host and mate location by the Sea Louse, Caligus rogercresseyi Boxshall & Bravo, 2000 (Copepoda: Caligidae). Aquacult 271:70–76

    Article  Google Scholar 

  • Plaisance L, Knowlton N, Paulay G, Meyer C (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28:977–986

    Article  Google Scholar 

  • Poore GCB, Bruce NL (2012) Global diversity of marine isopods (except Asellota and crustacean symbionts). PLoS One 7:e43529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popp BN, Graham BS, Olson RJ, Hannides CC, Lott MJ, López-Ibarra GA, Galván-Magaña F, Fry B (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. Terr Ecol 1:173–190

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Morand S (2000) The diversity of parasites. Q Rev Biol 75:277–293

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Curtis MA, Rau ME (1990) Responses of the fish ectoparasite Salmincola edwardsii (Copepoda) to stimulation, and their implication for host-finding. Parasitology 100:417–421

    Article  PubMed  Google Scholar 

  • Poulin R, Blasco-Costa I, Randhawa HS (2016) Integrating parasitology and marine ecology: seven challenges towards greater synergy. J Sea Res 113:3–10

    Article  Google Scholar 

  • Power M, Klein GM (2004) Fish host–cestode parasite stable isotope enrichment patterns in marine, estuarine and freshwater fishes from Northern Canada. Isotope Environ Health Stud 40:257–266

    Article  CAS  Google Scholar 

  • 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 Wildl 5:217–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Qviller L, Risnes-Olsen N, Bærum KM, Meisingset EL, Loe LE, Ytrehus B, Viljugrein H, Mysterud A (2013) Landscape level variation in tick abundance relative to seasonal migration in red deer. PLoS One 8:e71299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rameshkumar G, Ravichandran S, Sivasubramanian K (2013) Secondary microbial infection in carangid fishes due to cymothoid isopod parasites. Proc Natl Acad Sci 36:591–597

    CAS  Google Scholar 

  • Rines KM (2015) New Hampshire Moose Assessment 2015. New Hampshire Fish and Game Department Report

    Google Scholar 

  • Robinson MP (2005) Role of the isopod Anilocra partiti in the health, behavior and mating success of the bicolor damselfish, Stegastes bipartitus. Dissertation, University of Miami

    Google Scholar 

  • Roche DG, Binning SA, Strong LE, Davies JN, Jennions MD (2013a) Increased behavioural lateralization in parasitized coral reef fish. Behav Ecol Sociobiol 67:1339–1344

    Article  Google Scholar 

  • Roche DG, Strong LE, Binning SA (2013b) Prevalence of the parasitic cymothoid isopod Anilocra nemipteri on its fish host at Lizard Island, Great Barrier Reef. Aust J Zool 60:330–333

    Article  Google Scholar 

  • Rohde K (1976) Species diversity of parasites on the Great Barrier Reef. Parasitol Res 50:93–94

    Google Scholar 

  • Rohr JR, Swan A, Raffel TR, Hudson PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159:447–454

    Article  PubMed  Google Scholar 

  • Saarinen M, Taskinen J (2005) Long-lasting effect of stress on susceptibility of a freshwater clam to copepod parasitism. Parasitology 130:523–529

    Article  CAS  PubMed  Google Scholar 

  • Sala-Bonzano M, Van Oosterhou C, Mariani S (2012) Impact of a mouth parasite in a marine fish differs between geographical areas. Biol J Linnean Soc 105:842–852

    Article  Google Scholar 

  • Santos TRN, Sikkel PC (2017) Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines. Mar Biodivers 49:83–96. https://doi.org/10.1007/s12526-017-0756-6

    Article  Google Scholar 

  • Sasal P, Mouillot D, Fichez R, Chifflet S, Kulbicki M (2007) The use of fish parasites as biological indicators of anthropogenic influences in coral-reef lagoons: a case study of Apogonidae parasites in New-Caledonia. Marine Poll Bull 54:1697–1706

    Article  CAS  Google Scholar 

  • Sato T, Egusa T, Fukushima K, Oda T, Ohte N, Tokuchi N, Watanabe K, Kanaiwa M, Murakami I, Lafferty KD (2012) Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioral manipulation of their cricket hosts. Ecol Lett 15:786–793

    Article  PubMed  Google Scholar 

  • Schultz ET, Topper M, Heins DC (2006) Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect? Oikos 114:303–310

    Article  Google Scholar 

  • Sellers JC, Holstein DJ, Botha T, Sikkel PC (2019) Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes. Oecologia 189(2):293–305. https://doi.org/10.1007/s00442-018-4262-8

    Article  PubMed  Google Scholar 

  • Shantz AA, Ladd MC, Shrack E, Burkpile DE (2015) Fish-derived nutrient hotspots shape coral reef benthic communities. Ecol Appl 8:2142–2152

    Article  Google Scholar 

  • Shaw AK, Binning SA (2016) Migratory recovery from infection as a selective pressure for the evolution of migration. Am Nat 187:491–501

    Article  PubMed  Google Scholar 

  • Sikkel PC (1986) Intraspecific cleaning by juvenile salema, Xenestius californiensis (Pisces: Haemulidae). Calif Fish Game 72:170–172

    Google Scholar 

  • Sikkel PC, Kramer DL (2006) Territory revisits reduce intrusion during spawning trips by female yellowtail damselfish. Anim Behav 71:71–78

    Article  Google Scholar 

  • Sikkel PC, Smit NJ (2018) Intraspecific cleaning by juvenile Cape white seabream Diplodus capensis (Sparidae) off eastern South Africa. Afr J Mar Sci 40:97–99

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in marine reef fish. Anim Behav 68:241–247

    Article  Google Scholar 

  • Sikkel PC, Herzlieb SE, Kramer DL (2005) Compensatory cleaner-seeking behavior following spawning in female yellowtail damselfish. Mar Ecol Prog Ser 296:1–11

    Article  Google Scholar 

  • Sikkel PC, Schaumburg C, Mathenia J (2006) Diel infestation patterns of gnathiid isopod larvae on Caribbean reef fishes. Coral Reefs 25:683–689

    Article  Google Scholar 

  • Sikkel PC, Ziemba RE, Sears W, Wheeler J (2009) Ontogenetic shifts in timing of host infestation by parasitic gnathiid isopod larvae on Caribbean coral reefs. Coral Reefs 28:489–495

    Article  Google Scholar 

  • Sikkel PC, Sears WT, Weldon B, Tuttle BC (2011) An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod and a new technique for sampling gnathiids on coral reefs. Mar Biol 158:1075–1083

    Article  Google Scholar 

  • Sikkel PC, Tuttle LJ, Cure K, Coile AM, Hixon MA (2014) Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite. PLoS One 9:5

    Article  CAS  Google Scholar 

  • Sikkel PC, Welicky RL, Artim JM, McCammon AM, Sellers JC, Coile AM, Jenkins WG (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull Mar Sci 2:475–489

    Article  Google Scholar 

  • Smit NJ, Davies AJ (1999) New host records for Haemogregarina bigemina Laveran & Mesnil, 1901 (Apicomplexa; Adeleina) from South Africa. J Mar Biol Assoc UK 79:933–935

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Smit NJ, Bruce NL, Hadfield KA (2014) Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Int J Parasitol Parasites Wildl 3:188–197

    Article  PubMed  PubMed Central  Google Scholar 

  • Sonnenholzner JI, Lafferty KD, Ladah LB (2011) Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos. Ecology 92:2276–2284

    Article  PubMed  Google Scholar 

  • Stapp P, Salkeld DJ (2009) Inferring host–parasite relationships using stable isotopes: implications for disease transmission and host specificity. Ecology 90:3268–3273

    Article  PubMed  Google Scholar 

  • Stephenson AB (1976) Gill damage in fish produced by buccal parasites. Rec Auckland Inst Mus 13:167–173

    Google Scholar 

  • Stepien CA, Brusca RC (1985) Nocturnal attacks on nearshore fishes in southern California by crustacean zooplankton. Mar Biol 25:91–105

    Google Scholar 

  • Strathmann RR, Hughes TP, Kuris AM, Lindeman KC, Morgan SG, Pandolfi JM, Warner RR (2002) Evolution of local recruitment and its consequences for marine populations. Bull Mar Sci 70(Suppl 1):377–396

    Google Scholar 

  • Strauss A, White A, Boots M (2012) Invading with biological weapons: the importance of disease-mediated invasions. Funct Ecol 26:1249–1261

    Article  Google Scholar 

  • Sukhdeo MV (2010) Food webs for parasitologists: a review. J Parasitol 96:273–284

    Article  PubMed  Google Scholar 

  • Sun D, Blomberg SP, Cribb TH, McCormick MI, Grutter AS (2012) The effects of parasites on early life stages of a damselfish. Coral Reefs 31:1065–1075

    Article  Google Scholar 

  • Sures B, Siddall R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15:16–21

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tanaka K (2003) Population dynamics of the sponge-dwelling gnathiid isopod Elaphognathia cornigera. J Mar Biol Assoc UK 83:95–102

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Tanaka K, Aoki M (2000) Seasonal trait of reproduction in a gnathiid isopod Elaphognathia cornigera (Nunomura, 1992). Zool Sci 17:467–475

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Taskinen J, Saarinen M (1999) Increased parasite abundance associated with reproductive maturity of the clam Anodonta piscinalis. J Parasitol 85:588–591

    Article  CAS  PubMed  Google Scholar 

  • Terborgh J, Estes JA (2010) Trophic cascades: predators, prey, and the changing dynamics in nature. Island Press, Washington, DC

    Google Scholar 

  • Thieltges DW, Reise K, Prinz K, Jensen KT (2008) Invaders interfere with native parasite–host interactions. Biol Invasions 11:1421–1429

    Article  Google Scholar 

  • Thresher RE (1984) Reproduction in reef fishes. T.F.H. Publications, Neptune City

    Google Scholar 

  • Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345

    Article  Google Scholar 

  • 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(9):187

    Article  CAS  Google Scholar 

  • Tully O, Nolan DT (2002) A review of the population biology and host–parasite interactions of the sea louse Lepeophtheirus salmonis (Copepoda: Caligidae). Parasitology 124:S165–S182

    Article  PubMed  Google Scholar 

  • Tuttle LJ, Sikkel PC, Cure K, Hixon MA (2017) Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (Pterois volitans). Biol Invasions 19(2):563–575

    Article  Google Scholar 

  • Upton NPD (1987a) Gregarious larval settlement within a restricted intertidal zone and sex differences in subsequent mortality in the polygynous saltmarsh isopod Paragnathia formica (Crustacea: Isopoda). J Mar Biol Assoc UK 67:663–678

    Article  Google Scholar 

  • Upton NPD (1987b) Asynchronous male and female life cycles in the sexually dimorphic, harem–forming isopod Paragnathia formica (Crustacea: Isopoda). J Zool 212:677–690

    Article  Google Scholar 

  • Vaughan DB, Grutter AS, Costello MJ, Hutson KS (2017) Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses. Fish Fish 18:698–716

    Article  Google Scholar 

  • Wägele JW (1987) Description of the postembryonal stages of the Antarctic fish parasite Gnathia calva Vanhoffen (Crustacea: Isopoda) and synonymy with Heterognathia Amar & Roman. Polar Biol 7:77–92

    Article  Google Scholar 

  • Wagner GN, Fast MD, Johnson SC (2008) Physiology and immunology of Lepeophtheirus salmonis infections of salmonids. Trends Parasitol 24:76–183

    Article  CAS  Google Scholar 

  • Welbergen J (2006) Timing of the evening emergence from day roosts of the grey–headed flying fox, Pteropuspolioc ephalus: the effects of predation risk, foraging needs, and social context. Behav Ecol Sociobiol 60:311–322

    Article  Google Scholar 

  • Welicky RL, Sikkel PC (2014) Variation in occurrence of the fish–parasitic cymothoid isopod, Anilocra haemuli, infecting French grunt (Haemulon flavolineatum) in the north–eastern Caribbean. Mar Freshw Res 65:1018–1026

    Article  CAS  Google Scholar 

  • Welicky RL, Sikkel PC (2015) Decreased movement related to parasite infection in a diel migratory coral reef fish. Behav Ecol Sociobiol 69:1437–1446

    Article  Google Scholar 

  • Welicky RM, Cheney KL, Coile AM, McCammon A, Sikkel PC (2013) Lunar periodicity of activity of ectoparasitic gnathiid isopods on Caribbean coral reefs. Mar Biol 160:1607–1617

    Article  Google Scholar 

  • Welicky RL, Hadfield KA, Sikkel PC, Smit NJ (2017a) Molecular assessment of three species of Anilocra (Isopoda, Cymothoidae) ectoparasites from Caribbean coral reef fishes, with the description of Anilocra brillae sp. n. ZooKeys 663:21–43

    Article  Google Scholar 

  • Welicky RL, Demopoulos AWJ, Sikkel PC (2017b) Host-dependent differences in resource use associated with Anilocra spp. parasitism in two coral reef fishes, as revealed by stable carbon and nitrogen isotope analyses. Mar Ecol 38:e12413

    Article  CAS  Google Scholar 

  • Welicky RL, Ferreira ML, Sikkel PC, Smit NJ (2018a) Diurnal activity patterns of the temporary fish ectoparasite, Gnathia africana Barnard, 1914 (Isopoda, Gnathiidae), from the southern coast of South Africa. J Mar Biol Assoc UK 98:1715–1723

    Article  Google Scholar 

  • Welicky RL, Malherbe W, Hadfield KA, Smit NJ (2019) Understanding growth relationships of African cymothoid fish parasitic isopods using specimens from museum and field collections. Int J Parasitol: Parasites Wildl 8:182–187

    Google Scholar 

  • Welicky RL, Parkyn DC, Sikkel PC (2018b) Host-dependent differences in measures of condition associated with Anilocra spp. parasitism in two coral reef fishes. Environ Biol Fish 101:1223–1234

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Williams JD, Boyko CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscidea). PLoS One 7(4):1–9

    Article  CAS  Google Scholar 

  • Williams EH Jr, Bunkley-Williams L (1996) Parasites of off shore, big game sport fishes of Puerto Rico and the Western North Atlantic (Puerto Rico Department of Natural and Environmental Resources: San Juan, Department of Biology, University of Puerto Rico: Mayaguez)

    Google Scholar 

  • Williams EH Jr, Williams LB, Waldner RE, Kimmel JJ (1982) Predisposition of a pomacentrid fish, Chromis multilineatus (Guichenot) to parasitism by a cymothoid isopod, Anilocra chromis Williams and Williams. J Parasitol 1:942–945

    Article  Google Scholar 

  • Williams HH, MacKenzie K (2003) Marine parasites as pollution indicators: an update. Parasitology 126(7):S27–S41

    Article  CAS  PubMed  Google Scholar 

  • Wood CL, Lafferty KD (2015) How have fisheries affected parasite communities? Parasitology 142:134–144

    Article  PubMed  Google Scholar 

  • Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH (2007) Parasites alter community structure. Proc Natl Acad Sci USA 104:9335–9339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wood CL, Sandin SA, Zgliczynski B, Guerra AS, Micheli F (2014) Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance. Ecology 95:1929–1946

    Article  PubMed  Google Scholar 

  • Yahel R, Yahel G, Genin A (2005) Near-bottom depletion of zooplankton over coral reefs: I: Diurnal dynamics and size distribution. Coral Reefs 24:75–85

    Article  Google Scholar 

  • Rachel L. Welicky, Wynand Malherbe, Kerry A. Hadfield, Nico J. Smit, (2019) Understanding growth relationships of African cymothoid fish parasitic isopods using specimens from museum and field collections. International Journal for Parasitology: Parasites and Wildlife 8:182-187

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the multitude of collaborators, students and volunteers who have assisted with our research over the years, which would not have been possible without the generous financial support of the US National Science Foundation, Puerto Rico Sea Grant, Earthwatch Institute, the Falconwood Corporation, the National Research Foundation of South Africa and the Claude Leon Foundation of South Africa. Many thanks go to the NOAA Okeanos Explorer Program, Andrea M. Quattrini and Amanda W.J. Demopoulos for the images used in Fig. 10.9. We are also extremely grateful to the staff of the field stations where we have conducted our research, including the University of the Virgin Islands MacLean Marine Science Center, Virgin Islands Environmental Resource Station, UPRM Isla Magueyes Marine Laboratory, Guana Island, Silliman University Marine Laboratory and Lizard Island Research Station. Finally, we thank the editors of this book and the anonymous reviewers whose critiques and suggestions contributed significantly to the improvement of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biological Sciences and Environmental Sciences Program, Arkansas State University, Jonesboro, AR, USA

    Paul C. Sikkel & Rachel L. Welicky

  2. Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    Paul C. Sikkel & Rachel L. Welicky

  3. School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA

    Rachel L. Welicky

Authors
  1. Paul C. Sikkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachel L. Welicky
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. North-West University, and Unit for Environmental Sciences and Management , Potchefstroom, Northwest, South Africa

    Nico J. Smit

  2. Biodiversity & Geosciences Program, Queensland Museum, South Brisbane BC, Queensland 4101, Australia, and Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    Niel L. Bruce

  3. Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    Kerry A. Hadfield

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sikkel, P.C., Welicky, R.L. (2019). The Ecological Significance of Parasitic Crustaceans. In: Smit, N., Bruce, N., Hadfield, K. (eds) Parasitic Crustacea. Zoological Monographs, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-030-17385-2_10

Download citation

Publish with us

Policies and ethics

Search

Navigation