Abstract
Predation on parasites is an important ecological process, but few experimental studies have examined the long-term impacts on the prey. Cleaner fish prey upon large numbers and selectively feed on the larger individuals of the ectoparasitic stage of gnathiid isopods. Removal of cleaner fish Labroides dimidiatus for 1.5–12.5 years negatively affects coral reef fishes, but the mechanism is unclear. A reduction in local parasite populations or the size of individual parasites would benefit all susceptible fishes. We tested whether cleaner presence reduces local gnathiid populations using 18 patch-reefs distributed between two sites (both at Lizard Island, Great Barrier Reef) which were maintained cleaner-free or undisturbed for 12 years. Using emergence traps (1 m2), free-living gnathiid stages were sampled before and after cleaner fish were removed during the day and night, up to 11 times over the course of the experiment. There were effects of the removal in the predicted direction, driven largely by the response at one site over the other involving 200% more gnathiids, but manifested only in the daytime sampling after 4 months. There was also a main effect (36%) for the shared sample dates at both sites after 12 years. Gnathiid size occasionally differed with cleaner presence, but in no consistent way over time. Contrary to our predictions, changes in free-living gnathiid population numbers and their size structure rarely reflected the changes in fish populations and individuals observed on cleaner-free reefs. Therefore, evidence that this predator alone regulates gnathiids remains limited, suggesting other contributing processes are involved.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alldredge AL, King JM (1977) Distribution, abundance, and substrate preferences of demersal reef zooplankton at Lizard Island Lagoon, Great Barrier Reef. Mar Biol 41:317–333
Artim JM, Sikkel PC (2013) Live coral repels a common reef fish ectoparasite. Coral Reefs 32:487–494. https://doi.org/10.1007/s00338-012-0995-8
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. https://doi.org/10.5343/bms.2015.1023
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 36:1213–1223. https://doi.org/10.1007/s00338-017-1613-6
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593. https://doi.org/10.1146/annurev.ecolsys.38.091206.095818
Becker JH, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515–520. https://doi.org/10.1007/s00338-004-0429-3
Binning SA et al (2018) Cleaner wrasse indirectly affect the cognitive performance of a damselfish through ectoparasite removal. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.2447
Brown BL, Creed RP, Skelton J, Rollins MA, Farrell KJ (2012) The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments. Oecologia 170:199–207. https://doi.org/10.1007/s00442-012-2280-5
Bshary R (2003) The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. J Anim Ecol 72:169–176
Cantor M, Longo OG, Fontoura L, Quimbayo JP, Floeter SR, Bender MG (2018) Interaction networks in tropical reefs. In: Dattilo W, Rico-Grey V (eds) Ecological networks in the tropics. Springer, Cham, pp 141–154
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
Cheney KL, Bshary R, Grutter AS (2008) Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations. Behav Ecol 19:1063–1067. https://doi.org/10.1093/beheco/arn067
Clague GE, Cheney KL, Goldizen 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. https://doi.org/10.1098/rsbl.2011.0458
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. https://doi.org/10.1016/j.ijpara.2012.11.012
Dobson AP, May RM (1987) The effects of parasites on fish populations—theoretical aspects. Int J Parasitol 17:363–370
Finley RA, Forrester GE (2003) Impact of ectoparasites on the demography of a small reef fish. Mar Ecol Prog Ser 248:305–309
Fournier DA et al (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249
Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks
Gorlick DL, Atkins PD, Losey GS (1987) Effect of cleaning by Labroides dimidiatus (Labridae) on an ectoparasite population infecting Pomacentrus vaiuli (Pomacentridae) at Enewetak Atoll. Copeia 1:41–45
Grutter AS (1995) The relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58
Grutter AS (1996a) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70
Grutter AS (1996b) Experimental demonstration of no effect by the cleaner wrasse Labroides dimidiatus (Cuvier and Valenciennes) on the host fish Pomacentrus moluccensis (Bleeker). J Exp Mar Biol Ecol 196:285–298. https://doi.org/10.1016/0022-0981(95)00135-2
Grutter AS (1997a) Spatiotemporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997:346–355
Grutter AS (1997b) Effect of the removal of cleaner fish on the abundance and species composition of reef fish. Oecologia 111:137–143
Grutter AS (1997c) Size-selective predation by the cleaner fish Labroides dimidiatus. J Fish Biol 50:1303–1308
Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673. https://doi.org/10.1038/19443
Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proc R Soc Lond Ser B Biol Sci 268:1361–1365. https://doi.org/10.1098/rspb.2001.1658
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. https://doi.org/10.3354/meps259295
Grutter AS (2012) Enhanced colonization success and competition associated with conspecifics in cleaner fish Labroides dimidiatus juveniles. Coral Reefs 31:1169–1176. https://doi.org/10.1007/s00338-012-0942-8
Grutter AS, Lester RJG (2002) Cleaner fish Labroides dimidiatus reduce ‘temporary’ corallanid isopods on the coral reef fish Hemigymnus melapterus. Mar Ecol Prog Ser 234:247–255
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. https://doi.org/10.3354/meps164263
Grutter AS, Murphy JM, Choat JH (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67. https://doi.org/10.1016/s0960-9822(02)01393-3
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. https://doi.org/10.3354/meps207123
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. https://doi.org/10.1111/j.1365-2435.2010.01798.x
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. https://doi.org/10.1007/s00338-016-1537-6
Grutter AS et al (2018) Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37:15–24. https://doi.org/10.1007/s00338-017-1628-z
Hatcher MJ, Dunn AM (2011) Parasites in ecological communities: from interactions to cosystems. Cambridge University Press, Cambridge
Hopkins SR, Ocampo JM, Wojdak JM, Belden LK (2016) Host community composition and defensive symbionts determine trematode parasite abundance in host communities. Ecosphere 7:10. https://doi.org/10.1002/ecs2.1278
Hopkins SR, Wojdak JM, Belden LK (2017) Defensive symbionts mediate host-parasite interactions at multiple scales. Trends Parasitol 33:53–64. https://doi.org/10.1016/j.pt.2016.10.003
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
Johnson PTJ et al (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371. https://doi.org/10.1016/j.tree.2010.01.005
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. https://doi.org/10.1111/j.0022-1112.2005.00640.x
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. https://doi.org/10.1007/s00227-006-0416-z
Jones CM, Grutter AS (2008) Reef-based micropredators reduce the growth of post-settlement damselfish in captivity. Coral Reefs 27:677–684. https://doi.org/10.1007/s00338-008-0383-6
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. https://doi.org/10.1016/j.ijpara.2007.01.011
Koller M (2016) robustlmm: an R package for robust estimation of linear mixed-effects models. J Stat Softw 75:1–24. https://doi.org/10.18637/jss.v075.i06
Kuris AM, Lafferty KD (2000) Parasite-host modelling meets reality: adaptive peaks and their ecological attributes. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host-parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 9–26
Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216
Lewis EE, Campbell JF, Sukhdeo MVK (2002) The behavioural ecology of parasites. CABI Publishing, New York
Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74
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
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Raffaelli D, Moller H (2000) Manipulative field experiments in animal ecology: do they promise more than they can deliver? Adv Ecol Res 30(30):299–338
Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618. https://doi.org/10.1016/j.tree.2008.06.015
Rohde K (2005) Marine parasitology. CABI Publishing, Oxon
Salo P, Banks PB, Dickman CR, Korpimaki E (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecol Monogr 80:531–546. https://doi.org/10.1890/09-1260.1
Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities—a review of field experiments. Annu Rev Ecol Syst 16:269–311
Sikkel PC et al (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull Mar Sci 93:475–489. https://doi.org/10.5343/bms.2016.1021
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. https://doi.org/10.1007/s00338-009-0474-z
Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2016) Generalized linear mixed models using ‘AD Model Builder’. R package version 0.8.3.3 2016-01-19
Skelton J et al (2013) Servants, scoundrels, and hitchhikers: current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida). Freshw Sci 32:1345–1357. https://doi.org/10.1899/12-198.1
Smit NJ, Van As JG, Davies AJ (2003) Taxonomic re-evaluation of the South African fish haemogregarine, Desseria fragilis. J Parasitol 89:151–153
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. https://doi.org/10.1645/ge-756r.1
Soares MC, Oliveira RF, Ros AFH, Grutter AS, Bshary R (2011) Tactile stimulation lowers stress in fish. Nat Commun 2:ncomms1547. https://doi.org/10.1038/ncomms1547
Sotomayor DA, Lortie CJ (2015) Indirect interactions in terrestrial plant communities: emerging patterns and research gaps. Ecosphere. https://doi.org/10.1890/es14-00117.1
Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246
Stoll S, Fruh D, Westerwald B, Hormel N, Haase P (2013) Density-dependent relationship between Chaetogaster limnaei limnaei (Oligochaeta) and the freshwater snail Physa acuta (Pulmonata). Freshw Sci 32:642–649. https://doi.org/10.1899/12-072.1
Sun D et al (2015) Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs. Biol Lett. https://doi.org/10.1098/rsbl.2015.0456
Sun D et al (2016) Cleaner wrasse influence habitat selection of young damselfish. Coral Reefs 35:427–436. https://doi.org/10.1007/s00338-015-1391-y
Svavarsson J, Bruce NL (2012) New and little-known gnathiid isopod crustaceans (Cymothoida) from the northern Great Barrier Reef and the Coral Sea. Zootaxa 2012:1–33
Tanaka K (2007) Life history of gnathiid isopod-current knowledge and future directions. Plankton Benthos Res 2:1–11
Thieltges DW, Jensen KT, Poulin R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426. https://doi.org/10.1017/s0031182007000248
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. https://doi.org/10.1007/s00227-016-2959-y
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. https://doi.org/10.1111/faf.12198
Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS (2011) Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities. PLoS One 6:4. https://doi.org/10.1371/journal.pone.0021201
Wood CL, Lafferty KD (2015) How have fisheries affected parasite communities? Parasitology 142:134–144. https://doi.org/10.1017/s003118201400002x
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. https://doi.org/10.1111/j.1461-0248.2010.01467.x
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. https://doi.org/10.1890/13-1270.1
Acknowledgements
We thank N. Aurish, A. Crean, L. Curtis, B. Fargher, M.A. Johnson, C. Newport, T. Sinclair-Taylor, P. Waldie, M. De Brauwer, G. Marsden, I. Leiper, J. Vorse, P. Narvaez, numerous students and volunteers, and the Lizard Island Research Station staff for field assistance, L. Roman, R. Templin, and other volunteers for measuring the gnathiids, and N. J. Smit for a gnathiid identification.
Funding
The Australian Research Council (A00105175, A19937078, ARCFEL010G, DP0557058, DP120102415, ASG), the National Science Foundation (OCE1536794, PCS), Swiss Science Foundation Grant (3100A0120552, RB), Sea World Research and Rescue Foundation Australia (SWR22012, DS), and The University of Queensland funded this research.
Author information
Authors and Affiliations
Contributions
ASG conceived ideas and designed experiments, funded fieldwork, performed experiments, analysed the data, and led writing of the paper; SPB analysed some of the data and provided advice on statistical analyses; RB and PCS funded fieldwork and performed experiments; EMPM, MGM, RRW conceived ideas and designed experiments; ECM, JMM, DS, and CAS performed experiments; MAR wrote some of the methods; OH collected and analysed data, and created a figure. All authors provided editorial advice.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable institutional and/or national guidelines for the care and use of animals were followed.
Additional information
Communicated by Pieter Johnson.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Grutter, A.S., Blomberg, S.P., Box, S. et al. Changes in local free-living parasite populations in response to cleaner manipulation over 12 years. Oecologia 190, 783–797 (2019). https://doi.org/10.1007/s00442-019-04451-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04451-8