Access to Cleaning Services Alters Fish Physiology Under Parasite Infection and Ocean Acidification

Abstract

Cleaning symbioses are key mutualistic interactions where cleaners remove ectoparasites and tissues from client fishes. Such interactions elicit beneficial effects on clients’ ecophysiology, with cascading effects on fish diversity and abundance. Ocean acidification (OA), resulting from increasing CO2 concentrations, can affect the behavior of cleaner fishes making them less motivated to inspect their clients. This is especially important as gnathiid fish ectoparasites are tolerant to ocean acidification. Here, we investigated how access to cleaning services, performed by the cleaner wrasse Labroides dimidiatus, affect individual client’s (damselfish, Pomacentrus amboinensis) aerobic metabolism in response to both experimental parasite infection and OA. Access to cleaning services was modulated using a long-term removal experiment where cleaner wrasses were consistently removed from patch reefs around Lizard Island (Australia) for 17 years or left undisturbed. Only damselfish with access to cleaning stations had a negative metabolic response to parasite infection (maximum metabolic rate—ṀO2Max; and both factorial and absolute aerobic scope). Moreover, after an acclimation period of 10 days to high CO2 (∼1,000 µatm CO2), the fish showed a decrease in factorial aerobic scope, being the lowest in fish without the access to cleaners. We propose that stronger positive selection for parasite tolerance might be present in reef fishes without the access to cleaners, but this might come at a cost, as readiness to deal with parasites can impact their response to other stressors, such as OA.

The effects of climate change on the ecology of fishes

“…Some of these effects may be due to both dopaminergic and seratoninergic neurological impairment that for example can decrease the interactions between tropical cleaner wrasses (Labroides dimidiatus) and their client fishes (Naso elegans) in response to ocean warming and acidification conditions, thereby increasing the risk of parasites due to degradation of the cleaner-client mutualism [107]. Moreover, under acidification conditions, fish incur a significant metabolic cost when they do not have access to cleaning stations [108], which could increase vulnerability to parasites and disease. These responses become even more complex when the survival of some parasites (e.g., gnathids) is unaffected by ocean acidification conditions [109], thereby emphasizing the non-uniformity in responses within these relationships.…”

Impacts of acute hypoxia on the short-snouted seahorse metabolism and behaviour

“…Following previous methods (Clark et al, 2013;Paula et al, 2022;Rummer et al, 2016), an intermittent ow respirometry system was used for the measurement of the oxygen uptake rates (MO 2 ), applied to estimate the standard metabolic rates (SMR). Seahorses were individually placed in 606 ml (including tygon chemical tubing) respirometry chambers which were then completely closed so that there was no external in ltration of O 2 .…”

“…The initial period of 2 hours allowed acclimatization to the new environment and to the desired oxygen concentration in the hypoxia treatments. The total duration of the measurement period ensures that the O 2 levels inside the chambers never went below 80% air saturation (Paula et al, 2022) in the control treatment, ensuring that the measurements of MO 2 are not in uenced with any sharp metabolic decrease which may affect animal welfare. Between measurement periods, an automated ush pump submerged in a tank with treatment water supplied and renewed the chambers with clean seawater.…”

Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions

“…Cleaning mutualisms, one of the most beneficial interactions between fish species, is highly susceptible to environmental changes (Paula et al, 2019a;Paula, et al, 2019b;Paula et al, 2022;Paula et al, 2023;Triki et al, 2018). In particular, cleaning mutualisms are a crucial interaction on coral reef ecosystems consisting of the removal of ectoparasites and dead tissue from the skin of other fishes (known as 'clients'), enhancing their health and survival (Bshary & Côté, 2008;Grutter, 1999).…”