FCT Project - ChangingMoods

Abstract
Understanding the impacts of environmental change on ecological communities is a current societal challenge. In the marine realm, environmental perturbations such as climate change (CC) and extreme events (e.g. heatwaves) are predicted to affect ecosystems negatively. In coral reefs, most fishes engage in crucial cooperative cleaning interactions with cleaner fish. Cleaners remove ectoparasites, dead skin and mucus from client fishes. Cleaner wrasses, Labroides spp., are arguably the most studied group of cleaner fishes due to their vast distribution and notorious strategic cognitive sophistication. Within this cleaning mutualism system, a major conflict is present since cleaners prefer to eat the protective mucus from their clients, which constitutes cheating. This is the likely cause for the evolution of highly sophisticated decision-rules used by cleaners during interactions, including reconciliation, reputation management and social tool-use. Moreover, when cleaners have simultaneous invitations for inspection by multiple clients, they prioritise visitor clients with access to alternative cleaners over residents with access to the local cleaner only. This decision rule increases their food intake as visitors would use their partner choice options and switch to another cleaner if ignored, while the residents have to wait . Our team was able to translate the cleaners decision rule to a cognitive laboratory test, which allowed for the development of comparative cognition studies, showing that cleaners can outperform various primate species. The importance of cleaner wrasses in marine ecosystems is well-known, and our team has previously demonstrated that cleaning interactions have enormous effects on marine ecosystems. Cleaning interactions are known to be drivers of fish richness and abundance, highlighting cleaner fishes' ecological relevance in reef ecosystem stability. In the past four years, mass behavioural shifts were observed in reef fishes worldwide, due to environmental change. In other words, following environmental stress, adult cleaners stop displaying the previously documented strategic sophistication that made them a prime example for fish intelligence. However, cleaners' early-stage and transgenerational sensitivity to environmental change and how these behavioural abnormalities could impact the complete ecosystems remain unknown. The potential for ecosystem disruption due to cleaning behaviour abnormalities is substantial as the simple removal of cleaner fishes from coral reefs can lead to overfishing-type impacts on fish abundance and diversity. Additionally, the urgency of understanding how marine ecosystems deal with ongoing environmental change and the dependency of developing nations on coral reef ecosystems makes this project of utmost importance. The overall objective of this 3-year research project is to understand the ecological relevance and susceptibility of cleaner fish strategic sophistication and cooperative behaviour to environmental change. To achieve this objective, we need to know how cleaners develop their strategic sophistication (in an ontogenetic and transgenerational approach), how resilient is their strategic sophistication facing environmental stress and how fish communities respond to the absence of cleaner fish strategic sophistication. This research project relies on an integrative approach using mesocosms, ontogenetic and cognitive/behavioural ecology tools (Task 2); transgenerational crossings (T. 3); laboratory simulations of environmental stress (T. 4); neurobiology and neurogenomic tools (T. 5); large in situ ecological experiments (T. 6) and deep learning tools (T. 7). To ensure this project's success, we have gathered the expertise of a multidisciplinary team of national and international researchers, congregating top experts in the fields of marine ecology, behaviour, neurobiology, physiology, and genomics.

Published outputs:

M Ranucci, M Court, BP Pereira, D Romeo, JR Paula (2024) Cleaner gobies can solve a biological market task when the correct cue is larger. Frontiers Ecology & Evolution 12:1375835. 

J. Kang, S Ramirez-Calero, J.R. Paula, Y. Chen, C. Schunter (2023) Gene losses, parallel evolution and heightened expression confer adaptations to dedicated cleaning behaviour. BMC Biology 21, 180 DOI: 10.1186/s12915-023-01682-3

K. Rose, K. Holsman, J. Nye, E. Markowitz, T. Banha, N. Bednaršek, J. Bueno-Pardo, D. Deslauriers, E. Fulton, K. Huebert, M. Huret, S. Ito, S. Koenigstein, L. Li, H. Moustahfid, B. Muhling, P. Neubauer, J. R. Paula, E. Siddon, … M. Peck (2024). Advancing bioenergetics-based modeling to improve climate change projections of marine ecosystems. Marine Ecology Progress Series, 732, 193–221. https://doi.org/10.3354/meps14535

J. R. Paula, L. Cascalheira, R. Oliveira, E. Otjacques, C. Frazão-Santos, R. Beldade, S. C. Mills, R. Rosa (2023) GABAergic role in the disruption of wild cleaner fish behaviour under high CO2. Animal Behaviour 195, 77-84. DOI: 10.1016/j.anbehav.2022.11.003

B P Pereira, R Oliveira, MD Martins, R Rosa, JR Paula (2025), Ocean deoxygenation and warming disrupt cooperation in coral reef fish mutualisms, Behavioral Ecology, araf152, https://doi.org/10.1093/beheco/araf152 

B. Pereira, L. Cascalheira, R. Rosa, JR Paula (2025). Alteration of cleaner wrasse cognition and brain morphology under marine heatwaves. Functional Ecology, 00, 1–12. https://doi.org/10.1111/1365-2435.70014

J.R. Paula, X. Wang, C. Xu, D.C. Moreira (2023) Editorial: The defense responses of aquatic animals to the environment. Frontiers in Physiology 14, 1231014.DOI: 10.3389/fphys.2023.1231014

S. Ramirez-Calero, J.R.Paula, E. Otjacques, T. Ravasi, R. Rosa, C. Schunter (2023) Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions.  BMC Biol 21, 258 (2023). https://doi.org/10.1186/s12915-023-01761-5

S. Ramírez-Calero, J. R. Paula, E. Otjacques, R. Rosa, T. Ravasi, C. Schunter (2022) Neuro-molecular characterization of fish cleaning interactions. Scientific Reports 12, 8468. DOI: 10.1038/s41598-022-12363-6

J. R. Paula, T. Repolho, A.S. Grutter, R.Rosa (2022) Access to cleaning services alters fish physiology under parasite infection and ocean acidification. Frontiers in Physiology 13, 859556. DOI: 10.3389/fphys.2022.859556