ARTICLE https://doi.org/10.1038/s41467-020-17450-8 OPEN Anthropogenic stressors impact fish sensory development and survival via thyroid disruption ✉ Marc Besson 1,2,3 , William E. Feeney 4,5,6, Isadora Moniz1, Loïc François 1, Rohan M. Brooker 7, Guillaume Holzer 8, Marc Metian 3, Natacha Roux1,2, Vincent Laudet 2,10,11 & David Lecchini1,9,11 Larval metamorphosis and recruitment represent critical life-history transitions for most teleost fishes. While the detrimental effects of anthropogenic stressors on the behavior and 1234567890():,; survival of recruiting fishes are well-documented, the physiological mechanisms that underpin these patterns remain unclear. Here, we use pharmacological treatments to high- light the role that thyroid hormones (TH) play in sensory development and determining anti- predator responses in metamorphosing convict surgeonfish, Acanthurus triostegus. We then show that high doses of a physical stressor (increased temperature of +3 °C) and a chemical stressor (the pesticide chlorpyrifos at 30 µgL−1) induced similar defects by decreasing fish TH levels and affecting their sensory development. Stressor-exposed fish experienced higher predation; however, their ability to avoid predation improved when they received supple- mental TH. Our results highlight that two different anthropogenic stressors can affect critical developmental and ecological transitions via the same physiological pathway. This finding provides a unifying mechanism to explain past results and underlines the profound threat anthropogenic stressors pose to fish communities. 1 PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE BP 1013, 98729 Papetoai, Moorea, French Polynesia. 2 Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université, 1 Avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France. 3 International Atomic Energy Agency - Environment Laboratories, 4a Quai Antoine 1er, Principality of Monaco 98000, Monaco. 4 Environmental Futures Research Institute, Griffith University, Nathan, Australia. 5 Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany. 6 Department of Zoology, University of Cambridge, Cambridge, UK. 7 Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, VIC, Australia. 8 Institut de Génomique Fonctionnelle de Lyon, ENS Lyon, Lyon, France. 9 Laboratoire d’Excellence “CORAIL”, Moorea, French Polynesia. 10Present address: Marine Eco-Evo-Devo unit, Okinawa Institute for Science and Technology (OIST), 1919-1 Tancha, Onna-son, ✉ Okinawa 904-0495, Japan. 11These authors contributed equally: Vincent Laudet, David Lecchini. email: [email protected] NATURE COMMUNICATIONS | (2020) 11:3614 | https://doi.org/10.1038/s41467-020-17450-8 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-17450-8 he variety, frequency, and amplitude of anthropogenic settlement-stage A. triostegus (day 0 = d0, Fig. 1a) were collected stressors faced by organisms is unprecedented and at night, while they were moving from the pelagic environment to T 1,2 11 increasing . The scale of human activities has led to once the reef, using a crest net . Following capture, they were main- localized perturbations, such as heat waves3 and waterborne che- tained for up to 8 days (d8) in in situ cages, during which they mical toxicants4 becoming issues of global importance. Exposure to fully completed metamorphosis11. The olfactory, visual, and stressors can directly impact how organisms function and also mechanosensory structures (Fig. 1b–d) showed rapid develop- decrease their resilience to further exposure or exposure to other ment from d0 to d8 in control individuals, with the development stressors, resulting in cascading negative repercussions for them and of new lamellae, a 50% increase in bipolar cell density in the the ecosystem they inhabit5,6. The negative impacts of anthro- retina, and a 240% surge in trunk canal pore density, respectively pogenic stressors can be felt by all organisms at all life stages; (Fig. 1e–g). We investigated the role of TH in the development of however, aquatic species may be more vulnerable than terrestrial these sensory structures by injecting fish daily from d0 to d5 with 7 + organisms . Further, disruptions at critical life-history transitions, different pharmacological drugs: (i) T3 iopanoic acid (T3 such as during metamorphosis8, can disproportionately threaten the treatment) to achieve TH signal activation, and (ii) NH3 (a TH structure of communities and persistence of species9. antagonist, N3 treatment) to achieve TH signal disruption11. The Teleost fishes represent almost half of the world’s vertebrates and T3 treatment induced an accelerated development of all three generally exhibit a metamorphic transition from their larval to sensory structures, with elevated densities of bipolar cells at d2, as juvenile phase10,11. In marine species, such as coral and temperate well as elevated number of lamellae and greater density trunk reef fishes, this transition typically occurs as larvae move from the canal pores at both d2 and d5 (Fig. 1e–g). In contrast, N3-treated pelagic environment to their juvenile/adult reef-associated habitat, fish experienced repressed sensory development, at both d2 and i.e., recruitment11. The sensory systems of many recruiting fishes d5 for the retina and the olfactory organ (Fig. 1e, f), and at d2 for undergo rapid development as they metamorphose, which may help the trunk canal (Fig. 1g). Supplemental T3 rescued olfactory them locate and navigate toward suitable settlement habitats12,13, organ development in N3-treated fish (Supplementary Fig. 1). and survive during this life-history transition14,15. Nevertheless, fishes often experience an extreme predation bottleneck during TH signaling modulates behavioral responses to predator sti- recruitment; for instance, recruiting coral-reef fishes have an esti- muli and vulnerability to predation. As predation is high in the mated average mortality rate of 30% per day as a result of preda- 2 days following settlement in reef fishes16, we examined the tion16. Myriad recent studies have reported that various behavioral outcomes of different sensory structure developmental anthropogenic stressors, such as artificial light pollution17, – states by testing whether d0 and d2 control, T3-, and N3-treated increasing temperature18 20, ocean acidification21,22,sound fish responded differently when presented with chemical and pollution23,24, and waterborne chemical pollutants11,14,25 can lead visual cues from a common reef predator: the blacktail snapper, to the deterioration of ecologically important behaviors, including Lutjanus fulvus. In chemical choice experiments, d2 control fish the ability to detect predators and avoid predation. Predators and showed a clear avoidance of predator cues (Fig. 2a). This response prey do not appear to be equally affected by anthropogenic stres- was similar in T3-treated fish, while N3-treated fish did not sors21, suggesting that alterations to predator–prey dynamics have – discriminate between water sources, similar to d0 fish (Fig. 2a). the potential to drastically reshape fish communities26 28.Despite When comparing responses to visual cues in a separated aqua- this, our understanding of the mechanism(s) that underpin the rium, we again found that d2 control and T3-treated fish avoided patterns reported in these studies remains limited29,30. predator cues, while N3-treated fish showed no preference, The endocrine system plays an important role in post- similar to d0 fish (Fig. 2b). To investigate whether this inability to embryonic developmental processes8,31. In teleost fishes, meta- identify predation risk makes them more vulnerable to predation, morphosis is controlled by thyroid hormones (TH), including we conducted a predation test in an in situ arena. We found that thyroxine (T ) and triiodothyronine (T )10. Environmental 4 3 d2 T3-treated fish exhibited significantly higher survival (i.e., stressors (e.g., decreasing water level and food deprivation) and number of fish that survived) than d2 control fish, while d2 N3- anthropogenic stressors (e.g., waterborne chemical pollutants) treated fish exhibited lower survival than d2 control fish (Fig. 2c). have the ability to disrupt thyroid function, which can affect the timing, duration, and completion of metamorphic processes32,33. Surprisingly, the ultimate consequences of stressor-induced Increased temperature and chlorpyrifos affect TH levels and developmental and endocrine impairments, such as their sensory development. To examine whether independent expo- impact on predator–prey dynamics, remain poorly studied34.TH sure to two anthropogenic stressors can affect TH levels and plays a key role in neurogenesis and sensory development in sensory system development, we exposed A. triostegus from d0 to vertebrates35,36, and are central for regulating recruitment in reef d2 to increased temperature and to the organophosphate pesti- fishes11. Thus, TH signaling disruption may present a general- cide chlorpyrifos (CPF). Fish were exposed to either: (i) water at izable physiological mechanism through which reports of beha- 28.5 °C (control), 30.0 °C ( + 1.5 °C), or 31.5 °C ( + 3.0 °C), fol- vioral and survival deteriorations in recruiting fishes following lowing end-of-century projections for the tropical Pacific37; or (ii) exposure to anthropogenic stressors can be understood34. water containing no CPF (control),