- Email: [email protected]
Marine Life Cycle: A Polluted Terra Incognita Is Unveiled
Current Biology
Dispatch 6. Tilney, L.G., Tilney, M.S., and DeRosier, D.J. (1992). Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu. Rev. Cell Biol. 8, 257–274. 7. Belyantseva, I.A., Boger, E.T., Naz, S., Frolenkov, G.I., Sellers, J.R., Ahmed, Z.M., Griffith, A.J., and Friedman, T.B. (2005). MyosinXVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat. Cell Biol. 7, 148–156. 8. Manor, U., Disanza, A., Grati, M., Andrade, L., Lin, H., Di Fiore, P.P., Scita, G., and Kachar, B. (2011). Regulation of stereocilia length by myosin XVa and whirlin depends on the actinregulatory protein Eps8. Curr. Biol. 21, 167–172. 9. Zampini, V., Ruttiger, L., Johnson, S.L., Franz, C., Furness, D.N., Waldhaus, J., Xiong, H., Hackney, C.M., Holley, M.C., Offenhauser, N., et al. (2011). Eps8 regulates hair bundle length and functional maturation of mammalian auditory hair cells. PLoS Biol. 9, e1001048. 10. Tarchini, B., Tadenev, A.L., Devanney, N., and Cayouette, M. (2016). A link between planar polarity and staircase-like bundle architecture in hair cells. Development 143, 3926–3932. 11. Mauriac, S.A., Hien, Y.E., Bird, J.E., Carvalho, S.D., Peyroutou, R., Lee, S.C., Moreau, M.M., Blanc, J.M., Geyser, A., Medina, C., et al.
(2017). Defective Gpsm2/Galphai3 signalling disrupts stereocilia development and growth cone actin dynamics in Chudley-McCullough syndrome. Nat. Commun. 8, 14907. 12. Mitchem, K.L., Hibbard, E., Beyer, L.A., Bosom, K., Dootz, G.A., Dolan, D.F., Johnson, K.R., Raphael, Y., and Kohrman, D.C. (2002). Mutation of the novel gene Tmie results in sensory cell defects in the inner ear of spinner, a mouse model of human hearing loss DFNB6. Hum. Mol. Genet. 11, 1887–1898. 13. Zhao, B., Wu, Z., Grillet, N., Yan, L., Xiong, W., Harkins-Perry, S., and Muller, U. (2014). TMIE is an essential component of the mechanotransduction machinery of cochlear hair cells. Neuron 84, 954–967.
polymerization in stereocilia. Proc. Natl. Acad. Sci. USA 108, 5825–5830. 16. Velez-Ortega, A.C., Freeman, M.J., Indzhykulian, A.A., Grossheim, J.M., and Frolenkov, G.I. (2017). Mechanotransduction current is essential for stability of the transducing stereocilia in mammalian auditory hair cells. eLife 6, e24661. 17. Narayanan, P., Chatterton, P., Ikeda, A., Ikeda, S., Corey, D.P., Ervasti, J.M., and Perrin, B.J. (2015). Length regulation of mechanosensitive stereocilia depends on very slow actin dynamics and filament-severing proteins. Nat. Commun. 6, 6855.
14. Beurg, M., Fettiplace, R., Nam, J.H., and Ricci, A.J. (2009). Localization of inner hair cell mechanotransducer channels using highspeed calcium imaging. Nat. Neurosci. 12, 553–558.
18. Zhang, D.S., Piazza, V., Perrin, B.J., Rzadzinska, A.K., Poczatek, J.C., Wang, M., Prosser, H.M., Ervasti, J.M., Corey, D.P., and Lechene, C.P. (2012). Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481, 520–524.
15. Caberlotto, E., Michel, V., Foucher, I., Bahloul, A., Goodyear, R.J., Pepermans, E., Michalski, N., Perfettini, I., Alegria-Prevot, O., Chardenoux, S., et al. (2011). Usher type 1G protein sans is a critical component of the tiplink complex, a structure controlling actin
19. Drummond, M.C., Barzik, M., Bird, J.E., Zhang, D.S., Lechene, C.P., Corey, D.P., Cunningham, L.L., and Friedman, T.B. (2015). Live-cell imaging of actin dynamics reveals mechanisms of stereocilia length regulation in the inner ear. Nat. Commun. 6, 6873.
Marine Life Cycle: A Polluted Terra Incognita Is Unveiled Jean-Franc¸ois Ghiglione1 and Vincent Laudet2
1Observatoire Oce anologique de Banyuls-sur-Mer, UMR CNRS 7621 LOMIC, Sorbonne Universite , 1 avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France 2Observatoire Oce anologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Universite , 1 avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France Correspondence: [email protected] (J.-F.G.), [email protected] (V.L.) https://doi.org/10.1016/j.cub.2019.11.083
Teleost fishes have a biphasic life cycle, with pelagic larvae dispersing in the open ocean and juveniles or adults living in reef or coastal environments. A recent study reveals that fish larvae concentrate in a specific oceanic compartment, the surface slicks, which are polluted by microplastics that can be ingested by most larvae. Because we are terrestrial mammals of macroscopic size we very often neglect the incredible diversity of the living world around us. This diversity culminates in the sea, from which most metazoan phyla originate. But we also often forget that the diversity of animal forms must be extended to their ontogenic stages, and, again, this is particularly true for marine animals [1]. The vast majority of marine animals, including teleost fishes,
exhibit a biphasic life cycle with one (or several) larval planktonic stages and juvenile/adult stages that occur in a different ecological niche [2,3]. The existence of two distinct phases during the life cycle ensures the dispersion of individuals due to oceanic currents that convey these pelagic stages. It also reduces the predation level, which could be very high in coastal environments, such as coral reefs, and
R130 Current Biology 30, R112–R133, February 3, 2020 ª 2019 Elsevier Ltd.
ensures access to a large food source in plankton [4]. A large number of studies have addressed the entry of larval fish to their juvenile environments, often called settlement or recruitment [5]. In the case of coral reef fishes, this step is easy to recognize as it corresponds with the passing of the reef crest and the selection of an adequate microhabitat. In pelagic fishes, this step is less easy to follow, but
Current Biology
Dispatch Precipitation
Solar radiation Wind
Sea surface slicks
Aerosols
Evaporation
Gas exchanges (CO2’ O2’ CH4’ N2) Turbulence
Bubble production
Phytoplankton EF = 1.7
Zooplankton EF = 3.7
Fish larvae EF = 8.1
Bacteria and viruses
Hydrophobic persistant organic pollutants (POPs) and antibiotics
1m depth
Hydrophobic surfactant
Sea surface layer
Microplastic EF = 126
Current Current Biology
Figure 1. Natural sea water slicks. These structures formed under calm weather conditions are enriched in phytoplankton, zooplankton and fish larvae, but also in microplastic that may have adverse effects on the entire trophic chain. EF: enrichment factor in surface slick as compared with ambient water, with indicated values coming from [11].
it coincides with the transformation of the larvae into active swimmers that often, like tuna, form a shoal. In any case, this step corresponds to a complete transformation of a larva into a juvenile — a metamorphosis that is triggered by thyroid hormones [2,6]. The distribution of larvae in the open ocean remains almost a complete mystery, a terra incognita. Where are larvae in the ocean? How are they distributed in the water column? We know now that fish in the late larval stage are much more active than anticipated and are certainly not passive propagules following the currents [7]. Thanks to many studies using plankton nets to better understand the vertical distribution of plankton, we have had several glimpses into their presence in different levels of the water column. However, apart from the observation that they follow the regular diel vertical migration of plankton [8] and that some species often use algal rafts floating on the surface [9], we know almost nothing about the life of oceanic fish larvae [10]. A recent and fascinating analysis by Gove et al. [11], however, brings some news and exciting information on fish
larvae in the open ocean and reveals an astonishing complexity. Sadly, this study also reveals that, despite the tremendous dilution power of the oceanic volume of water, fish larvae reside in an extremely polluted compartment. Let’s start with the fascinating side of the story. In the western portion of Hawai’i, which is the most protected site from winds, Gove et al. [11] have performed an extensive series (>100) of plankton net tows, searching for fish larvae and focusing on the neuston, the compartment of plankton that lives close to the surface. They observed that the density of plankton was variable from one plankton trait to another, and they realized that planktonic animals, including fish larvae, were more frequent in surface slicks than in the neighboring ambient waters. Sea surface slicks are formed under calm weather conditions by the accumulation of hydrophobic organic compounds that protrude at the surface, thus creating a film referred to as a ‘slick’ when visible that affects the physical and optical properties of the sea surface [12,13] (Figure 1). These structures aggregate the planktonic organisms that
are the base of the marine food web [14]. Gove et al. [11] have carefully mapped the extent of these labile structures close to Hawai’i west shores and have observed that they form a dynamic network roughly parallel to the shore. Most importantly, Gove et al. [11] found that the densities of phytoplankton (measured by chlorophyll content), zooplankton and fish larvae are effectively higher (1.7-, 3.7- and, strikingly 8.1-fold, respectively) in surface slicks than in ambient waters. Clearly, larval fish would benefit from the accumulation of planktonic organisms. Interestingly, they observed that the overall distance between two such surface slicks is 500 m, a distance that can easily be crossed by a fish larva that is capable of actively swimming [7]. In total, they observed that the surface slick represented 8.3% of all nearshore waters at the time of their observations, and that they contained 42% of all surface fish larvae. The authors therefore suggest that the convergence of surface waters underlying the surface slicks aggregates the marine organisms that are at the base of the oceanic food chain, creating a gradient of plankton which is, of course,
Current Biology 30, R112–R133, February 3, 2020 R131
Current Biology
Dispatch attractive for fish larvae that probably converge passively and actively in these structures. As the surface is also the vital ‘skin’ of the ocean, linking the water and the atmosphere, these structures may also have other specific features in terms of oxygen content, organic matter content, light filtering, or UV ray penetrance that provide selective advantage [12,13]. Gove et al. [11] have carefully studied the taxonomic composition of the fish larvae encountered in those slicks and have observed that they belong to a wide variety of fish taxa whose adults live in a variety of habitats. They found larvae of large pelagic fish such as swordfish, mahi-mahi or flying fish at an astonishing 28-fold higher density but they also found more demersal species such as jacks, goatfish, as well as deep-water mesopelagic fish such as lanternfish and even some coral reef fishes such as triggerfish. It is clear from their data that there is a hidden complexity here since the authors observed a difference in the respective amount of the various types of fish in the surface slicks versus the ambient waters. For example, they observed that slicks contain 50% pelagic fishes and 45% of coral reef fishes, whereas the ambient waters contain mostly (73.6%) coral reef fishes and only 15.3% of pelagic fishes. Coupled with the observation that surface slicks contain more fish larvae of more than 8 mm of size, this suggests that fish larvae choose the compartment that they prefer. Are coral fish larvae avoiding these surface slicks because of a higher predation level? Are pelagic fish larvae, especially the older, and therefore bigger ones, more active and therefore more able to fully exploit the opportunity offered by the concentration of plankton in the slicks? Could these differences be linked to a difference in maturity between waves of larvae produced by spawning events in coral reefs or in the pelagic ocean? How are these concentrations of organisms in surface slicks formed, and what happens to them during periods of strong winds that disrupt these structures? Do the fish smell the concentration of organic matters and plankton to actively swim toward those slicks? All these questions are still unresolved and are exciting avenues to explore in future studies. Once again, this reinforces the notion that fish
larvae are active animals that have their own behavior and have constantly vital choices to make. This fascinating story also has, however, an upsetting aspect. Indeed, Gove et al. [11] show that the processes forming the surface slicks and concentrating phytoplankton and zooplankton also concentrate buoyant microplastic particles present in the ocean. They observed that microplastics were present at a 126-fold higher concentration in surface slicks than in ambient water. Overall, their results suggest that 91% of the plastic particles present in the surface area were found in the sea surface slicks, probably due to their low density and hydrophobic properties. Microplastics in sea surface slicks were mainly composed of polyethylene (77%) and polypropylene (20%) with 41% being of the size of fish larval prey (<1 mm). Overall, the ratio between microplastics and fish larvae was inverted between surface slicks (7:1) and ambient water (1:2), fish larvae thus being more likely to ingest microplastics in surface slicks. Microplastics are not passively concentrated in surface slicks — they also more heavily contaminate the fish larvae present in these structures. After dissecting 658 larval fishes, Gove et al. [11] observed that larval fish captured in surface slicks are 2.3-fold more contaminated than larvae coming from ambient water. The authors observed mostly blue or translucent microfibers in the ingested plastics, suggesting that the fish larvae confuse the microplastic particles with their zooplanktonic prey items. These observations are really disturbing. Indeed, the fact that surface slicks host a large proportion of fish larvae suggests that these structures have a role as nurseries and are therefore critical for the replenishment of adult fish populations. This is likely to be of major importance since it concerns species critical in the food chain, such as flying fish, and most of them, such as swordfish or mahi-mahi (common dolphinfish), are consumed by humans. This critical compartment is also, however, heavily contaminated by microplastic particles that will not only dramatically obstruct the digestive tracts of the larvae but also contaminate
R132 Current Biology 30, R112–R133, February 3, 2020
them with the pollutants adsorbed in their surface. This is particularly the case in surface slicks where persistent organic pollutants (POPs) and antibiotics accumulate [15,16]. This is even more disquieting, as it is known that larval stages are very often the life stages most sensitive to endocrine disruptors known to be part of the composition of many plastic additives [17]. It has been shown that the thyroid hormone-controlled transformation of fish larvae into juveniles is effectively sensitive to endocrine disruption by pollutants [6] and that this step influences postmetamorphosis animal condition [18]. Microplastics are also known to host bacteria, the so-called ‘plastisphere’, which may cause diseases when ingested [19]. Many of us were expecting that plastic pollution would only affect fish living near the shore, owing to the immense dilution effect of the ocean. The analysis of Gove et al. [11], however, suggests that even in the pelagic realm the level of pollution by microplastics may be sufficient to affect a very sensitive, and vital, component of the marine ecological network. REFERENCES 1. Nielsen, C. (2012). Animal Evolution: Interrelationships of the Living Phyla, 3rd ed. (Oxford University Press). 2. Laudet, V. (2011). The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21, R726–R737. 3. McMenamin, S.K., and Parichy, D.M. (2013). Metamorphosis in teleosts. Curr. Top. Dev. Biol. 103, 127–165. 4. Jones, G.P., Almany, G.R., Russ, G.R., Sale, F., Steneck, R.S., van Oppen, M.J.H., and Willis, B.L. (2009). Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325. 5. Sponaugle, S. (2015). Recruitment of coral reef fishes: linkage across stages. In Ecology of Fishes on Coral Reefs, C. Mora, ed. (Cambridge Univ. Press), pp. 28–33. 6. Holzer, G., Besson, M., Lambert, A., Franc¸ois, L., Barth, P., Gillet, B., Hughes, S., Piganeau, G., Leulier, F., Viriot, L., et al. (2017). Fish larval recruitment to reefs is a thyroid hormonemediated metamorphosis sensitive to the pesticide chlorpyrifos. Elife 6, e27595. 7. Leis, J.M. (2006). Are larvae of demersal fishes plankton or nekton? Adv. Mar. Biol. 51, 57–141. 8. Neilson, J.D., and Perry, R.I. (1990). Diel vertical migration of marine fishes: An obligate or facultative process? Adv. Mar. Biol. 26, 115–168.
Current Biology
Dispatch 9. Thiel, M., and Gutow, L. (2005). The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceano. Mar. Biol. Annu. Rev. 43, 279–418. 10. Llopiz, J.K., Cowen, R.K., Hauff, M.J., Ji, R., Munday, P.L., Muhling, B.A., Peck, M.A., Richardson, D.E., Sogard, S., and Sponaugle, S. (2014). Early life history and fisheries oceanography: New questions in a changing world. Oceanography 27, 26–41. 11. Gove, J.M., Whitney, J.L., McManus, M.A., Lecky, J., Carvalho, F.C., Lynch, J.M., Li, J., Neubauer, P., Smith, K.A., Phipps, J.E., et al. (2019). Prey-size plastics are invading larval fish nurseries. Proc. Natl. Acad. Sci. USA 116, 24143–24149. 12. Zhang, Z., Liu, L., Liu, C., and Cai, W. (2003). Studies on the sea surface microlayer II. The layer of sudden change of physical and
chemical properties. J. Colloid Interface Sci. 264, 148–159. 13. Engel, A., Bange, H.W., Cunliffe, M., Burrows, S.M., Friedrichs, G., Galgani, L., Herrmann, H., Hertkorn, N., Johnson, M., Liss, P.S., et al. (2017). The ocean’s vital skin: Toward an integrated understanding of the sea surface microlayer. Front. Mar. Sci. 4, 165. 14. Kingsford, M.J., and Choat, J.H. (1986). Influence of surface slicks on the distribution and onshore movements of small fish. Marine Biol. Mar. Biol. 91, 161–171. 15. Ziccardi, L.M., Edgington, A., Hentz, K., Kulacki, K.J., and Kane Driscoll, S. (2016). Microplastics as vectors for bioaccumulation of hydrophobic organic chemicals in the marine environment: A state-of-the-science review. Env. Tox. Chem. 35, 1667–1676.
16. Li, J., Zhang, K., and Zhang, H. (2018). Adsorption of antibiotics on microplastics. Env. Poll. 237, 460–467. 17. Groh, K.J., Backhaus, T., Carney-Almroth, B., Geueke, B., Inostroza, P.A., Lennquist, A., Leslie, H.A., Maffini, M., Slunge, D., Trasande, T., et al. (2019). Overview of known plastic packaging-associated chemicals and their hazards. Sci. Total Env. 651, 3253–3268. 18. Hamilton, S.L. (2008). Larval history influences post-metamorphic condition in a coral-reef fish. Oecologia 158, 449–461. 19. Jacquin, J., Cheng, J., Odobel, C., Pandin, C., Conan, P., Pujo-Pay, M., Barbe, V., Meistertzheim, A.L., and Ghiglione, J.F. (2019). Microbial ecotoxicology of marine plastic debris: a review on colonization and biodegradation by the ‘plastisphere’. Front. Microbiol. 10, 865.
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Dispatch 6. Tilney, L.G., Tilney, M.S., and DeRosier, D.J. (1992). Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu. Rev. Cell Biol. 8, 257–274. 7. Belyantseva, I.A., Boger, E.T., Naz, S., Frolenkov, G.I., Sellers, J.R., Ahmed, Z.M., Griffith, A.J., and Friedman, T.B. (2005). MyosinXVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat. Cell Biol. 7, 148–156. 8. Manor, U., Disanza, A., Grati, M., Andrade, L., Lin, H., Di Fiore, P.P., Scita, G., and Kachar, B. (2011). Regulation of stereocilia length by myosin XVa and whirlin depends on the actinregulatory protein Eps8. Curr. Biol. 21, 167–172. 9. Zampini, V., Ruttiger, L., Johnson, S.L., Franz, C., Furness, D.N., Waldhaus, J., Xiong, H., Hackney, C.M., Holley, M.C., Offenhauser, N., et al. (2011). Eps8 regulates hair bundle length and functional maturation of mammalian auditory hair cells. PLoS Biol. 9, e1001048. 10. Tarchini, B., Tadenev, A.L., Devanney, N., and Cayouette, M. (2016). A link between planar polarity and staircase-like bundle architecture in hair cells. Development 143, 3926–3932. 11. Mauriac, S.A., Hien, Y.E., Bird, J.E., Carvalho, S.D., Peyroutou, R., Lee, S.C., Moreau, M.M., Blanc, J.M., Geyser, A., Medina, C., et al.
(2017). Defective Gpsm2/Galphai3 signalling disrupts stereocilia development and growth cone actin dynamics in Chudley-McCullough syndrome. Nat. Commun. 8, 14907. 12. Mitchem, K.L., Hibbard, E., Beyer, L.A., Bosom, K., Dootz, G.A., Dolan, D.F., Johnson, K.R., Raphael, Y., and Kohrman, D.C. (2002). Mutation of the novel gene Tmie results in sensory cell defects in the inner ear of spinner, a mouse model of human hearing loss DFNB6. Hum. Mol. Genet. 11, 1887–1898. 13. Zhao, B., Wu, Z., Grillet, N., Yan, L., Xiong, W., Harkins-Perry, S., and Muller, U. (2014). TMIE is an essential component of the mechanotransduction machinery of cochlear hair cells. Neuron 84, 954–967.
polymerization in stereocilia. Proc. Natl. Acad. Sci. USA 108, 5825–5830. 16. Velez-Ortega, A.C., Freeman, M.J., Indzhykulian, A.A., Grossheim, J.M., and Frolenkov, G.I. (2017). Mechanotransduction current is essential for stability of the transducing stereocilia in mammalian auditory hair cells. eLife 6, e24661. 17. Narayanan, P., Chatterton, P., Ikeda, A., Ikeda, S., Corey, D.P., Ervasti, J.M., and Perrin, B.J. (2015). Length regulation of mechanosensitive stereocilia depends on very slow actin dynamics and filament-severing proteins. Nat. Commun. 6, 6855.
14. Beurg, M., Fettiplace, R., Nam, J.H., and Ricci, A.J. (2009). Localization of inner hair cell mechanotransducer channels using highspeed calcium imaging. Nat. Neurosci. 12, 553–558.
18. Zhang, D.S., Piazza, V., Perrin, B.J., Rzadzinska, A.K., Poczatek, J.C., Wang, M., Prosser, H.M., Ervasti, J.M., Corey, D.P., and Lechene, C.P. (2012). Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481, 520–524.
15. Caberlotto, E., Michel, V., Foucher, I., Bahloul, A., Goodyear, R.J., Pepermans, E., Michalski, N., Perfettini, I., Alegria-Prevot, O., Chardenoux, S., et al. (2011). Usher type 1G protein sans is a critical component of the tiplink complex, a structure controlling actin
19. Drummond, M.C., Barzik, M., Bird, J.E., Zhang, D.S., Lechene, C.P., Corey, D.P., Cunningham, L.L., and Friedman, T.B. (2015). Live-cell imaging of actin dynamics reveals mechanisms of stereocilia length regulation in the inner ear. Nat. Commun. 6, 6873.
Marine Life Cycle: A Polluted Terra Incognita Is Unveiled Jean-Franc¸ois Ghiglione1 and Vincent Laudet2
1Observatoire Oce anologique de Banyuls-sur-Mer, UMR CNRS 7621 LOMIC, Sorbonne Universite , 1 avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France 2Observatoire Oce anologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Universite , 1 avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France Correspondence: [email protected] (J.-F.G.), [email protected] (V.L.) https://doi.org/10.1016/j.cub.2019.11.083
Teleost fishes have a biphasic life cycle, with pelagic larvae dispersing in the open ocean and juveniles or adults living in reef or coastal environments. A recent study reveals that fish larvae concentrate in a specific oceanic compartment, the surface slicks, which are polluted by microplastics that can be ingested by most larvae. Because we are terrestrial mammals of macroscopic size we very often neglect the incredible diversity of the living world around us. This diversity culminates in the sea, from which most metazoan phyla originate. But we also often forget that the diversity of animal forms must be extended to their ontogenic stages, and, again, this is particularly true for marine animals [1]. The vast majority of marine animals, including teleost fishes,
exhibit a biphasic life cycle with one (or several) larval planktonic stages and juvenile/adult stages that occur in a different ecological niche [2,3]. The existence of two distinct phases during the life cycle ensures the dispersion of individuals due to oceanic currents that convey these pelagic stages. It also reduces the predation level, which could be very high in coastal environments, such as coral reefs, and
R130 Current Biology 30, R112–R133, February 3, 2020 ª 2019 Elsevier Ltd.
ensures access to a large food source in plankton [4]. A large number of studies have addressed the entry of larval fish to their juvenile environments, often called settlement or recruitment [5]. In the case of coral reef fishes, this step is easy to recognize as it corresponds with the passing of the reef crest and the selection of an adequate microhabitat. In pelagic fishes, this step is less easy to follow, but
Current Biology
Dispatch Precipitation
Solar radiation Wind
Sea surface slicks
Aerosols
Evaporation
Gas exchanges (CO2’ O2’ CH4’ N2) Turbulence
Bubble production
Phytoplankton EF = 1.7
Zooplankton EF = 3.7
Fish larvae EF = 8.1
Bacteria and viruses
Hydrophobic persistant organic pollutants (POPs) and antibiotics
1m depth
Hydrophobic surfactant
Sea surface layer
Microplastic EF = 126
Current Current Biology
Figure 1. Natural sea water slicks. These structures formed under calm weather conditions are enriched in phytoplankton, zooplankton and fish larvae, but also in microplastic that may have adverse effects on the entire trophic chain. EF: enrichment factor in surface slick as compared with ambient water, with indicated values coming from [11].
it coincides with the transformation of the larvae into active swimmers that often, like tuna, form a shoal. In any case, this step corresponds to a complete transformation of a larva into a juvenile — a metamorphosis that is triggered by thyroid hormones [2,6]. The distribution of larvae in the open ocean remains almost a complete mystery, a terra incognita. Where are larvae in the ocean? How are they distributed in the water column? We know now that fish in the late larval stage are much more active than anticipated and are certainly not passive propagules following the currents [7]. Thanks to many studies using plankton nets to better understand the vertical distribution of plankton, we have had several glimpses into their presence in different levels of the water column. However, apart from the observation that they follow the regular diel vertical migration of plankton [8] and that some species often use algal rafts floating on the surface [9], we know almost nothing about the life of oceanic fish larvae [10]. A recent and fascinating analysis by Gove et al. [11], however, brings some news and exciting information on fish
larvae in the open ocean and reveals an astonishing complexity. Sadly, this study also reveals that, despite the tremendous dilution power of the oceanic volume of water, fish larvae reside in an extremely polluted compartment. Let’s start with the fascinating side of the story. In the western portion of Hawai’i, which is the most protected site from winds, Gove et al. [11] have performed an extensive series (>100) of plankton net tows, searching for fish larvae and focusing on the neuston, the compartment of plankton that lives close to the surface. They observed that the density of plankton was variable from one plankton trait to another, and they realized that planktonic animals, including fish larvae, were more frequent in surface slicks than in the neighboring ambient waters. Sea surface slicks are formed under calm weather conditions by the accumulation of hydrophobic organic compounds that protrude at the surface, thus creating a film referred to as a ‘slick’ when visible that affects the physical and optical properties of the sea surface [12,13] (Figure 1). These structures aggregate the planktonic organisms that
are the base of the marine food web [14]. Gove et al. [11] have carefully mapped the extent of these labile structures close to Hawai’i west shores and have observed that they form a dynamic network roughly parallel to the shore. Most importantly, Gove et al. [11] found that the densities of phytoplankton (measured by chlorophyll content), zooplankton and fish larvae are effectively higher (1.7-, 3.7- and, strikingly 8.1-fold, respectively) in surface slicks than in ambient waters. Clearly, larval fish would benefit from the accumulation of planktonic organisms. Interestingly, they observed that the overall distance between two such surface slicks is 500 m, a distance that can easily be crossed by a fish larva that is capable of actively swimming [7]. In total, they observed that the surface slick represented 8.3% of all nearshore waters at the time of their observations, and that they contained 42% of all surface fish larvae. The authors therefore suggest that the convergence of surface waters underlying the surface slicks aggregates the marine organisms that are at the base of the oceanic food chain, creating a gradient of plankton which is, of course,
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Dispatch attractive for fish larvae that probably converge passively and actively in these structures. As the surface is also the vital ‘skin’ of the ocean, linking the water and the atmosphere, these structures may also have other specific features in terms of oxygen content, organic matter content, light filtering, or UV ray penetrance that provide selective advantage [12,13]. Gove et al. [11] have carefully studied the taxonomic composition of the fish larvae encountered in those slicks and have observed that they belong to a wide variety of fish taxa whose adults live in a variety of habitats. They found larvae of large pelagic fish such as swordfish, mahi-mahi or flying fish at an astonishing 28-fold higher density but they also found more demersal species such as jacks, goatfish, as well as deep-water mesopelagic fish such as lanternfish and even some coral reef fishes such as triggerfish. It is clear from their data that there is a hidden complexity here since the authors observed a difference in the respective amount of the various types of fish in the surface slicks versus the ambient waters. For example, they observed that slicks contain 50% pelagic fishes and 45% of coral reef fishes, whereas the ambient waters contain mostly (73.6%) coral reef fishes and only 15.3% of pelagic fishes. Coupled with the observation that surface slicks contain more fish larvae of more than 8 mm of size, this suggests that fish larvae choose the compartment that they prefer. Are coral fish larvae avoiding these surface slicks because of a higher predation level? Are pelagic fish larvae, especially the older, and therefore bigger ones, more active and therefore more able to fully exploit the opportunity offered by the concentration of plankton in the slicks? Could these differences be linked to a difference in maturity between waves of larvae produced by spawning events in coral reefs or in the pelagic ocean? How are these concentrations of organisms in surface slicks formed, and what happens to them during periods of strong winds that disrupt these structures? Do the fish smell the concentration of organic matters and plankton to actively swim toward those slicks? All these questions are still unresolved and are exciting avenues to explore in future studies. Once again, this reinforces the notion that fish
larvae are active animals that have their own behavior and have constantly vital choices to make. This fascinating story also has, however, an upsetting aspect. Indeed, Gove et al. [11] show that the processes forming the surface slicks and concentrating phytoplankton and zooplankton also concentrate buoyant microplastic particles present in the ocean. They observed that microplastics were present at a 126-fold higher concentration in surface slicks than in ambient water. Overall, their results suggest that 91% of the plastic particles present in the surface area were found in the sea surface slicks, probably due to their low density and hydrophobic properties. Microplastics in sea surface slicks were mainly composed of polyethylene (77%) and polypropylene (20%) with 41% being of the size of fish larval prey (<1 mm). Overall, the ratio between microplastics and fish larvae was inverted between surface slicks (7:1) and ambient water (1:2), fish larvae thus being more likely to ingest microplastics in surface slicks. Microplastics are not passively concentrated in surface slicks — they also more heavily contaminate the fish larvae present in these structures. After dissecting 658 larval fishes, Gove et al. [11] observed that larval fish captured in surface slicks are 2.3-fold more contaminated than larvae coming from ambient water. The authors observed mostly blue or translucent microfibers in the ingested plastics, suggesting that the fish larvae confuse the microplastic particles with their zooplanktonic prey items. These observations are really disturbing. Indeed, the fact that surface slicks host a large proportion of fish larvae suggests that these structures have a role as nurseries and are therefore critical for the replenishment of adult fish populations. This is likely to be of major importance since it concerns species critical in the food chain, such as flying fish, and most of them, such as swordfish or mahi-mahi (common dolphinfish), are consumed by humans. This critical compartment is also, however, heavily contaminated by microplastic particles that will not only dramatically obstruct the digestive tracts of the larvae but also contaminate
R132 Current Biology 30, R112–R133, February 3, 2020
them with the pollutants adsorbed in their surface. This is particularly the case in surface slicks where persistent organic pollutants (POPs) and antibiotics accumulate [15,16]. This is even more disquieting, as it is known that larval stages are very often the life stages most sensitive to endocrine disruptors known to be part of the composition of many plastic additives [17]. It has been shown that the thyroid hormone-controlled transformation of fish larvae into juveniles is effectively sensitive to endocrine disruption by pollutants [6] and that this step influences postmetamorphosis animal condition [18]. Microplastics are also known to host bacteria, the so-called ‘plastisphere’, which may cause diseases when ingested [19]. Many of us were expecting that plastic pollution would only affect fish living near the shore, owing to the immense dilution effect of the ocean. The analysis of Gove et al. [11], however, suggests that even in the pelagic realm the level of pollution by microplastics may be sufficient to affect a very sensitive, and vital, component of the marine ecological network. REFERENCES 1. Nielsen, C. (2012). Animal Evolution: Interrelationships of the Living Phyla, 3rd ed. (Oxford University Press). 2. Laudet, V. (2011). The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21, R726–R737. 3. McMenamin, S.K., and Parichy, D.M. (2013). Metamorphosis in teleosts. Curr. Top. Dev. Biol. 103, 127–165. 4. Jones, G.P., Almany, G.R., Russ, G.R., Sale, F., Steneck, R.S., van Oppen, M.J.H., and Willis, B.L. (2009). Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325. 5. Sponaugle, S. (2015). Recruitment of coral reef fishes: linkage across stages. In Ecology of Fishes on Coral Reefs, C. Mora, ed. (Cambridge Univ. Press), pp. 28–33. 6. Holzer, G., Besson, M., Lambert, A., Franc¸ois, L., Barth, P., Gillet, B., Hughes, S., Piganeau, G., Leulier, F., Viriot, L., et al. (2017). Fish larval recruitment to reefs is a thyroid hormonemediated metamorphosis sensitive to the pesticide chlorpyrifos. Elife 6, e27595. 7. Leis, J.M. (2006). Are larvae of demersal fishes plankton or nekton? Adv. Mar. Biol. 51, 57–141. 8. Neilson, J.D., and Perry, R.I. (1990). Diel vertical migration of marine fishes: An obligate or facultative process? Adv. Mar. Biol. 26, 115–168.
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Dispatch 9. Thiel, M., and Gutow, L. (2005). The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceano. Mar. Biol. Annu. Rev. 43, 279–418. 10. Llopiz, J.K., Cowen, R.K., Hauff, M.J., Ji, R., Munday, P.L., Muhling, B.A., Peck, M.A., Richardson, D.E., Sogard, S., and Sponaugle, S. (2014). Early life history and fisheries oceanography: New questions in a changing world. Oceanography 27, 26–41. 11. Gove, J.M., Whitney, J.L., McManus, M.A., Lecky, J., Carvalho, F.C., Lynch, J.M., Li, J., Neubauer, P., Smith, K.A., Phipps, J.E., et al. (2019). Prey-size plastics are invading larval fish nurseries. Proc. Natl. Acad. Sci. USA 116, 24143–24149. 12. Zhang, Z., Liu, L., Liu, C., and Cai, W. (2003). Studies on the sea surface microlayer II. The layer of sudden change of physical and
chemical properties. J. Colloid Interface Sci. 264, 148–159. 13. Engel, A., Bange, H.W., Cunliffe, M., Burrows, S.M., Friedrichs, G., Galgani, L., Herrmann, H., Hertkorn, N., Johnson, M., Liss, P.S., et al. (2017). The ocean’s vital skin: Toward an integrated understanding of the sea surface microlayer. Front. Mar. Sci. 4, 165. 14. Kingsford, M.J., and Choat, J.H. (1986). Influence of surface slicks on the distribution and onshore movements of small fish. Marine Biol. Mar. Biol. 91, 161–171. 15. Ziccardi, L.M., Edgington, A., Hentz, K., Kulacki, K.J., and Kane Driscoll, S. (2016). Microplastics as vectors for bioaccumulation of hydrophobic organic chemicals in the marine environment: A state-of-the-science review. Env. Tox. Chem. 35, 1667–1676.
16. Li, J., Zhang, K., and Zhang, H. (2018). Adsorption of antibiotics on microplastics. Env. Poll. 237, 460–467. 17. Groh, K.J., Backhaus, T., Carney-Almroth, B., Geueke, B., Inostroza, P.A., Lennquist, A., Leslie, H.A., Maffini, M., Slunge, D., Trasande, T., et al. (2019). Overview of known plastic packaging-associated chemicals and their hazards. Sci. Total Env. 651, 3253–3268. 18. Hamilton, S.L. (2008). Larval history influences post-metamorphic condition in a coral-reef fish. Oecologia 158, 449–461. 19. Jacquin, J., Cheng, J., Odobel, C., Pandin, C., Conan, P., Pujo-Pay, M., Barbe, V., Meistertzheim, A.L., and Ghiglione, J.F. (2019). Microbial ecotoxicology of marine plastic debris: a review on colonization and biodegradation by the ‘plastisphere’. Front. Microbiol. 10, 865.
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