Abstract
Gnathiid isopods, common fish ectoparasites, can affect fish physiology, behaviour and survival. Gnathiid juveniles emerge from the benthos to feed on fish blood. In the Caribbean, gnathiids are positively associated with dead coral and negatively associated with live coral, due to coral predation on gnathiids. However, such interactions were unstudied in the Great Barrier Reef (GBR). Due to recent extreme weather events (two cyclones and one mass warm-water coral bleaching event, 2014–2016), it is now urgent to understand the role of corals on the abundance of these ectoparasites. Here, to understand parasite–coral dynamics at the micro-habitat level, we examined substrate associations of gnathiid isopods on Lizard Island (GBR) using demersal plankton emergence traps. Additionally, we determined whether two abundant hard coral species, Goniopora lobata and Pocillopora damicornis, predate on gnathiids in a laboratory experiment using containers with gnathiids and fragments from each coral species or dead coral as controls. The abundance of gnathiids over natural substrates was higher for dead compared to live hard coral and sand, but not live soft coral. Moreover, we found that free-swimming gnathiids decreased in containers with live coral compared to dead coral controls. This was attributed to predation as we also directly observed a coral ingesting a gnathiid. Our results suggest that dead coral is a suitable microhabitat for gnathiids, but that live coral is not since live corals can predate on gnathiids. We propose that following extreme events, such as cyclones and heat waves, gnathiids might benefit from more dead coral substrate and a decrease in predation by the reduction in coral cover on the reef. We advocate that an increase in the frequency of extreme events may have cascading effects for the fish population through changes in the population of benthos-dependent ectoparasites.
Similar content being viewed by others
Data availability
The datasets generated and analysed during this study are available in the Figshare repository: https://doi.org/10.6084/m9.figshare.12393794 (Paula et al. 2021).
References
Artim JM, Sikkel PC (2013) Live coral repels a common reef fish ectoparasite. Coral Reefs 32:487–494
Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlementstage reef fish in the eastern Caribbean Sea. Bull Mar Sci 91:479–487
Artim JM, Nicholson, MD, Hendrick GC, Brandt, M, Smith, T, Sikkel PC (2020) Abundance of a cryptic generalist parasite reflects degradation of an ecosystem. Ecosphere 11, e03268
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalised linear mixed modeling. The R Journal 9:378–400
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309
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
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
Fox J, Weisberg S (2011) An R Companion to Applied Regression. Sage, California
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser
Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70
Grutter AS (1997) Spatio-temporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997:346–355
Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673
Grutter AS (2002) Cleaning symbioses from the parasites’ perspective. Parasitology 124 Suppl:S65–81
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
Grutter AS, Glover S, Bshary R (2005) Does client size affect cleaner fish choice of client? An empirical test using client fish models. J Fish Biol 66:1748–1752
Grutter AS, Pickering JL, McCallum H, McCormick MI (2008) Impact of micropredatory gnathiid isopods on young coral reef fishes. Coral Reefs 27:655–661
Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, McCormick MI (2011) Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol 25:586–594
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
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
Grutter AS, Blomberg SP, Box S, Bshary R, Ho O, Madin EMP, McClure EC, Meekan MG, Murphy JM, Richardson MA, Sikkel PC, Sims CA, Sun D, Warner RR (2019) Changes in local free-living parasite populations in response to cleaner manipulation over 12 years. Oecologia 190:783–797
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 34:563–566
Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PPA, Hoogenboom MO, Kennedy E V., Kuo CY, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske S a, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–71
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
Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216
Lenth R (2020) Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.4. https://CRAN.R-project.org/package=emmeans
Lenz EA, Bramanti L, Lasker HR, Edmunds PJ (2015) Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34:1099–1109
Madin J, Baird A, Bridge T, Connolly S, Zawada K, Dornelas M (2018) Cumulative effects of cyclones and bleaching on coral cover and species richness at Lizard Island. Mar Ecol Prog Ser 604:263–268
Marino F, Giannetto S, Paradiso ML, Bottari T, De Vico G, Macrì B (2004) Tissue damage and haematophagia due to praniza larvae (Isopoda: Gnathiidae) in some aquarium seawater teleosts. Dis Aquat Organ 59:43–47
Mugride RER, Stallybrass HG (1983) A mortality of eels, Anguilla anguilla L., attributed to Gnathiidae. J Fish Dis 6:81–82
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
Nicholson MD, Artim JD, Hendrick GC, Packard AJ, Sikkel PC (2019) Fish-parasitic gnathiid isopods metamorphose following invertebrate-derived meal. J Parasitol 105:793
Pagán JA, Veríssimo A, Sikkel PC, Xavier R (2020) Hurricane-induced disturbance increases genetic diversity and population admixture of the direct-brooding isopod, Gnathia marleyi. Sci Rep 10, 8649
Palardy JE, Rodrigues LJ, Grottoli AG (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J Exp Mar Bio Ecol 367:180–188
Paula JR, Repolho T, Pegado MR, Thörnqvist PO, Bispo R, Winberg S, Munday PL, Rosa R (2019) Neurobiological and behavioural responses of cleaning mutualisms to ocean warming and acidification. Sci Rep 9:12728
Paula JR, Otjacques E, Hildebrandt C, Grutter AS, Rosa R (2020) Ocean acidification does not affect fish ectoparasite survival. Oceans 1:27–33
Paula JR, Sun D, Pissara V, Narvaez P, Rosa R, Grutter AS, Sikkel PC (2021) Data from: The role of corals on the abundance of a fish ectoparasite in the Great Barrier Reef. Figshare. https://doi.org/10.6084/m9.figshare.12393794
R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
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
Sellers JC, Holstein DM, Botha TL, Sikkel PC (2019) Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes. Oecologia 189:293–305
Shodipo MO, Gomez RDC, Welicky RL, Sikkel PC (2019) Apparent kleptoparasitism in fish—parasitic gnathiid isopods. Parasitol Res 118:653–655
Shodipo MO, Duong B, Graba-Landry A, Grutter AS, Sikkel PC (2020) Effect of acute seawater temperature increase on the survival of a fish ectoparasite. Oceans 1:215–236
Sikkel PC, Welicky R (2019) The Ecological Significance of Parasitic Crustaceans. In: Smit NJ, Bruce NL, Hadfield KA (eds) Parasitic Crustacea. Zoological Monographs Vol. 3. Springer, Cham
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
Sikkel PC, Herzlieb SE, Kramer DL (2005) Compensatory cleaner-seeking behavior following spawning in female yellowtail damselfish. Mar Ecol Prog Ser 296:1–11
Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689
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
Sikkel PC, Richardson MA, Sun D, Narvaez P, Feeney WE, Grutter AS (2019) Changes in abundance of fish-parasitic gnathiid isopods associated with warm-water bleaching events on the northern Great Barrier Reef. Coral Reefs 38:721–730
Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391
Sun, D, Cheney, KL, Werminghausen, J, McClure, EC, Meekan, MG, McCormick, MI, Cribb, TH, Grutter, AS (2016) Cleaner wrasse influence habitat selection of young damselfish. Coral Reefs 35:427–436
Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21
Tanaka K (2007) Life history of gnathiid isopods - current knowledge and future directions. Plankt Benthos Res 2:1–11
Triki Z, Bshary R (2019) Fluctuations in coral reef fish densities after environmental disturbances on the northern Great Barrier Reef. PeerJ 7:e6720
Triki Z, Grutter AS, Bshary R, Ros AFH (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163:187
Triki Z, Wismer S, Levorato E, Bshary R (2018) A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations. Glob Chang Biol 24:481–489
Zuur AF, Ieno EN, Walker N, Saveliev A, Smith G (2009) Mixed Effects Models and Extensions in Ecology with R. Springer-Verlag New York
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
Acknowledgements
The authors acknowledge field assistants and the staff of Lizard Island Research Station for their friendship and help during this study. Portuguese national funds funded this study through FCT–Fundação para a Ciência e Tecnologia, I.P., within the project PTDC/MAR-EST/5880/2014 (MUTUALCHANGE: Bio-ecological responses of marine cleaning mutualisms to climate change) to JRP and RR, the strategic project UID/MAR/04292/2013 and a PhD scholarship to JRP (SFRH/BD/111153/2015). Lizard Island Reef Research Foundation supported this study with a Lizard Island Doctoral Fellowship to JRP. United States National Science Foundation supported this study within the project OCE-1536794 to PCS and ASG. JRP is currently supported by project ASCEND—PTDC/BIA-BMA/28609/2017 co-funded by FCT–Fundação para a Ciência e Tecnologia, I.P, Programa Operacional Regional de Lisboa, Portugal 2020 and the European Union within the project LISBOA- 01-0145-FEDER-028609.
Author information
Authors and Affiliations
Contributions
JRP, RR, ASG and PS designed the study. JRP, DS, VP, PN, RR and PS performed the experiment and collected the data. JRP, RR, ASG and PS analysed the data. JRP, RR, ASG and PS wrote the manuscript. All authors discussed the results, their implications and commented on the manuscript at all stages.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Topic Editor Mark Vermeij
Supplementary Information
Rights and permissions
About this article
Cite this article
Paula, J.R., Sun, D., Pissarra, V. et al. The role of corals on the abundance of a fish ectoparasite in the Great Barrier Reef. Coral Reefs 40, 535–542 (2021). https://doi.org/10.1007/s00338-021-02051-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-021-02051-8