On coral reef systems, ‘client’ fishes combat relentless ectoparasitic infections by engaging in frequent mutualistic interactions with various ‘cleaner’ organisms. Clients are known to adjust their visits to cleaners according to their ectoparasite load. Whether physiological changes due to the ectoparasitic infection, prior to engaging in cleaning interactions, might inform clients of their current need to visit cleaners remains unclear. Here, we tested whether fish blood parameters vary with ectoparasitic infection: we exposed clients (Scolopsis bilineatus) to hematophagous ectoparasite gnathiid isopods (Gnathia aureamaculosa) or a control situation for 30 min, then collected fish blood and counted gnathiids attached to fish. We found that gnathiid-exposed fish had higher blood cortisol hormone levels compared with controls. This suggests gnathiid presence in the experimental situation results in an acute stress hormone response in a fish. In contrast, while hematocrit level, a correlate of blood loss, did not significantly differ between treatments, within gnathiid-exposed fish hematocrit was negatively related to attached gnathiid number. This suggests hematocrit could provide information to a fish about gnathiid load. Thus, short-term exposure to an ectoparasite translates into possible proximate physiological mechanisms underlying client’s decisions involving interactions with cleaners.
Cortisol Cortisol Level Parasite Load Hematocrit Level Fish Blood
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.
We thank the LIRS directors and staff for their support and friendship. We also thank D. Nusbaumer, S. Gingins, and D. Sun for their assistance, and G. Glauser and A. Vallat from the Chemical Analytical Service of the University of Neuchâtel for their assistance with MS-HPLC analysis.
This study was funded by the Australian Research Council (ASG and RB), the Swiss Science Foundation (RB), and the Swiss Scholarships for foreign students (ZT).
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest.
The University of Queensland Animal Ethics Committee approved the project.
Boots M, Sasaki A (2002) Parasite-driven extinction in spatially explicit host-parasite systems. Am Nat 159:706–713CrossRefGoogle Scholar
Bshary R, Grutter AS (2002) Experimental evidence that partner choice is a driving force in the payoff distribution among cooperators or mutualists: the cleaner fish case. Ecol Lett 5:130–136CrossRefGoogle Scholar
Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol 38:311–355Google Scholar
Dunlap KD, Mathies T (1993) Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 1993:1045. doi:10.2307/1447082CrossRefGoogle Scholar
Ebert D, Lipsitch M, Mangin KL (2000) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am Nat 156:459–477. doi:10.1086/303404CrossRefGoogle Scholar
Galhardo L, Oliveira RF (2009) Psychological stress and welfare in fish. Annu Rev Biomed Sci 11:1–20CrossRefGoogle Scholar
Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30CrossRefGoogle Scholar
Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58CrossRefGoogle Scholar
Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70CrossRefGoogle Scholar
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 259:295–302CrossRefGoogle Scholar
Grutter AS, Bshary R (2003) Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc R Soc Lond B Biol Sci 270:S242–S244CrossRefGoogle Scholar
Grutter A, 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. doi:10.1006/jfbi.2000.1312CrossRefGoogle Scholar
Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864CrossRefGoogle Scholar
Marino F, Giannetto S, Paradiso M et al (2004) Tissue damage and haematophagia due to praniza larvae (Isopoda: Gnathiidae) in some aquarium seawater teleosts. Dis Aquat Organ 59:43–47. doi:10.3354/dao059043CrossRefGoogle Scholar
Ros AFH, Lusa J, Meyer M et al (2011) Does access to the bluestreak cleaner wrasse Labroides dimidiatus affect indicators of stress and health in resident reef fishes in the Red Sea? Horm Behav 59:151–158. doi:10.1016/j.yhbeh.2010.11.006CrossRefGoogle Scholar
Ros AFH, Vullioud P, Bshary R (2012) Treatment with the glucocorticoid antagonist RU486 reduces cooperative cleaning visits of a common reef fish, the lined bristletooth. Horm Behav 61:37–43. doi:10.1016/j.yhbeh.2011.09.013CrossRefGoogle Scholar
Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. In: Advances in parasitology, vol 58. Academic Press, Elsevier, pp 289–391. doi:10.1016/S0065-308X(04)58005-3Google Scholar
St. Juliana JR, Khokhlova IS, Wielebnowski N et al (2014) Ectoparasitism and stress hormones: strategy of host exploitation, common host–parasite history and energetics matter. J Anim Ecol 83:1113–1123. doi:10.1111/1365-2656.12217CrossRefGoogle Scholar
Szabó K, Szalmás A, Liker A, Barta Z (2002) Effects of haematophagous mites on nestling house sparrows (Passer domesticus). Acta Parasitol 47:318–322Google Scholar
Wagner ELES, Roche DG, Binning SA et al (2015) Temporal comparison and predictors of fish species abundance and richness on undisturbed coral reef patches. PeerJ 3:e1459. doi:10.7717/peerj.1459CrossRefGoogle Scholar