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Magazine to the potential clinical applications, the availability of these tropomyosintargeting compounds has the potential to revolutionise our understanding of tropomyosin function. After many years in the background, tropomyosin is shaking off its monochrome image and providing individual colour to the different populations of actin filaments that it has created (Box 1). FURTHER READING Brayford, S., Bryce, N.S., Schevzov, G., Haynes, E.M., Bear, J.E., Hardeman, E.C., and Gunning, P.W. (2016). Tropomyosin promotes lamellipodial persistence by collaborating with Arp2/3 at the leading edge. Curr. Biol. 26, 1312–1318. Geeves, M.A., Hitchcock-DeGregori, S.E., and Gunning, P.W. (2015). A systematic nomenclature for mammalian tropomyosin isoforms. J. Muscle Res. Cell Motil. 36, 147–153. Gunning, P. (2008). Tropomyosin (Texas: Landes Bioscience.) Gunning, P.W., Ghoshdastider, U., Whitaker, S., Popp, D., and Robinson, R.C. (2015). The evolution of compositionally and functionally distinct actin filaments. J. Cell Sci. 128, 2009–2019. Gunning, P.W., Hardeman, E.C., Lappalainen, P., and Mulvihill, D.P. (2015). Tropomyosin — master regulator of actin filament function in the cytoskeleton. J. Cell Sci. 128, 2965–2974. Hsiao, J.Y., Goins, L.M., Petek, N.A., and Mullins, R.D. (2015). Arp2/3complex and cofilin modulate binding of tropomyosin to branched actin networks. Curr. Biol. 25, 1573–1582. Hundt, N., Steffen, W., Pathan-Chhatbar, S., Taft, M.H., and Manstein, D.J. (2016). Load-dependent modulation of non-muscle myosin-2A function by tropomyosin 4.2. Sci. Rep. 6, 20554. Johnson, M., East, D.A., and Mulvihill, D.P. (2014). Formins determine the functional properties of actin filaments in yeast. Curr. Biol. 24, 1525–1530. Schevzov, G., Whittaker, S.P., Fath, T., Lin, J.J.-C., and Gunning, P.W. (2011). Tropomyosin isoforms and reagents. BioArchitecture 1, 135–164. Sckolnick, M., Krementsova, E.B., Warshaw, D.M., and Trybus, K.M. (2016). Tropomyosin isoforms bias actin track selection by vertebrate myosin Va. Mol. Biol. Cell. 27, 2889–2897. Stehn, J.R., Haass, N.K., Bonello, T., Desouza, M., Kottyan, G., Treutlein, H., Zeng, J., Nascimento, P.R.B.B., Sequeira, V.B., Butler, T.L., et al. (2013). A novel class of anticancer compounds targets the actin cytoskeleton in cancer cells. Cancer Res. 73, 5169–5182. Tojkander, S., Gateva, G., Schevzov, G., Hotulainen, P., Naumanen, P., Martin, C., Gunning, P.W., and Lappalainen, P. (2011). A molecular pathway for myosin II recruitment to stress fibers. Curr. Biol. 21, 539–550. von der Ecken, J., Heissler, S.M., Pathan-Chhatbar, S., Manstein, D.J., and Raunser, S. (2015). Cryo-EM structure of a human cytoplasmic actomyosin complex at near-atomic resolution. Nature 534, 724–728. Wolfenson, H., Meacci, G., Liu, S., Stachowiak, M.R., Iskratsch, T., Ghassemi, S., Roca-Cusachs, P., O’Shaughnessy, B., Hone, J., and Sheetz, M.P. (2016). Tropomyosin controls sarcomere-like contractions for rigidity sensing and suppressing growth on soft matrices. Nat. Cell Biol. 18, 33–42.

School of Medical Sciences, University of New South Wales, Sydney, NSW, 2052, Australia. E-mail: [email protected] (P.W.G.), [email protected] (E.C.H.)

Correspondence

Can biological invasions save Caribbean coral reefs? David Roy Bellwood1,2,* and Christopher Harry Robert Goatley1 It is widely accepted that coral reefs are in decline globally, due to climate change as well as more direct human impacts such as poor water quality and overharvesting [1–3]. Biological invasions are also seen as a major threat [4–6]; however, they may not all be negative. An invasion of Red Sea rabbitfishes is disrupting Mediterranean ecosystems by removing macro-algae — meanwhile, in contrast, the Caribbean is suffering from excess macro-algal growth. We suggest that an invasion of the Caribbean by rabbitfishes may prove beneficial, and that the future of Caribbean coral reefs may depend upon a rabbitfish invasion. The invasions of lionfishes (Pterois volitans and P. miles) in the Caribbean and rabbitfishes (Siganus luridus and S. rivulatus) in the Mediterranean (Figure 1) are currently seen as ecological disasters. The Caribbean lionfish invasion has been identified as one of the world’s top conservation issues [5], highlighting the vulnerability of Caribbean coral reef ecosystems. Reduced herbivory, because of overharvesting of herbivorous fishes, and the loss of the sea urchin Diadema have led to region-wide algal outbreaks. These declines, combined with coral disease and storms, have resulted in the collapse of many Caribbean coral-reef ecosystems [3]. Lionfish species released into this compromised ecosystem expanded rapidly (Figure 1A), replacing overfished native predators and decimating populations of small fishes, including critically important herbivores [4] (Supplemental Information). Lionfishes are now major predators in the Caribbean. With the ability to further supress fish-based herbivory, they seem poised to shape the future of Caribbean coral reefs [4].

In a striking parallel, Mediterranean ecosystems are also undergoing profound changes as a result of invasions, with tropical species entering the eastern Mediterranean from the Red Sea (a process known as Lessepsian migration). Almost one hundred fish species have entered the Mediterranean by this route, and the numbers are still increasing [7,8]. Some of the most successful Lessepsian migrants are the rabbitfishes, S. rivulatus and S. luridus, which are now the dominant herbivorous fishes in the eastern Mediterranean [7]. Rabbitfishes have spread rapidly, and currently extend from the coast of Israel to France [9] (Figure 1A). The rabbitfishes have also been implicated in a major transformation of Mediterranean benthic ecosystems; their grazing activity appears to have triggered a major shift in the benthos by removing macroalgae. This has led to the proliferation of short algal turfs and a concomitant decline in populations of native herbivorous fishes such as the Salema porgy, Sarpa salpa (Sparidae), a fish species that traditionally feeds on seagrass and macroalgae. This ‘tropicalization’ of the Mediterranean is regarded as a major ecological problem [7,8]. We now have two degraded ecosystems: one herbivore depauperate and the other overburdened with herbivores. Both systems are being negatively impacted by invasive species that are rapidly expanding their geographic ranges. This raises the question: will rabbitfishes invade the Caribbean? There are several lines of evidence to suggest that this may occur. First, the geographic range of rabbitfishes has expanded rapidly, making them the dominant benthic herbivores in the eastern Mediterranean. Second, rabbitfishes appear to be particularly flexible in this new environment, with their only habitat requirement being a rocky shoreline. Moreover, they have already crossed most of the major biogeographic barriers within the Mediterranean [8], and further expansion along Mediterranean coasts and into the tropical and sub-tropical East Atlantic is anticipated [9]. Based on this evidence and current climatic trends [8,9], invasion of the Caribbean appears likely (Supplemental Information).

Current Biology 27, R1–R18, January 9, 2017 © 2017 Elsevier Ltd. R13

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Magazine AUTHOR CONTRIBUTIONS

A

Conceptualization: D.R.B., investigation and writing: D.R.B. and C.H.R.G. ACKNOWLEDGMENTS Funded by the Australian Research Council (DRB). REFERENCES

B

C

Figure 1. Invasions drive ecosystem change. (A) The rapid invasion of the Caribbean and Mediterranean, from first sightings (yellow stars) to present-day distributions (lionfishes P. volitans and P. miles shown in red; rabbitfishes S. rivulatus in orange and S. luridus in yellow; see Supplemental Information for data sources). (B) Lionfishes are denuding Caribbean coral reefs of small fishes, exacerbating reef decline. (C) Across the Atlantic, rabbitfishes have triggered ecosystem shifts throughout the eastern Mediterranean.

Approximately 20% of fish lineages in the Caribbean appear to have crossed the Atlantic from east to west [10], making invasion by rabbitfishes seem to be just a matter of time. Given the rapid expansion of these two groups of fishes, and the likelihood of accelerated expansion under future climate change [6,9], the question arises: what will happen if, or when, rabbitfishes cross the Atlantic? Remarkably, rabbitfishes may help save Caribbean coral reefs. Caribbean reefs are currently faced with overgrowth of by macroalgae, intense and relatively unconstrained human fishing pressure, severe habitat degradation, low coral cover, and expanding lionfish populations feeding on naïve prey [3,4]. Rabbitfishes could address all of these problems. Rabbitfishes rapidly remove macroalgae [7]. Although this is a problem in the Mediterranean, it may prove beneficial in the Caribbean. Furthermore, rabbitfishes can maintain their role as herbivores even under significant fishing pressure; they are already the focus of major fisheries in the Mediterranean and Indian Ocean yet remain significant contributors to herbivory [2,7]. Unlike Diadema, rabbitfish feeding has no negative R14

side effects such as grazing of coral recruits, and as Indo-Pacific species they are likely to be less vulnerable to lionfish predation than Caribbean species (Supplemental Information). Furthermore, as rabbitfishes have feeding traits that differ from other reef herbivores [1], they are unlikely to face significant competition for food on Caribbean reefs. Rabbitfish do not require corals — as demonstrated by their Mediterranean colonization — but they do remove algae from crevices, potentially improving surfaces for coral settlement and survival [1]. Rabbitfishes may thus facilitate coral reef growth. Although invasions are often undesirable, colonization of the Caribbean by rabbitfishes may help the recovery of coral reefs. This raises the issue of active interventions. Although such interventions are highly contentious [4–6] and are probably premature, this may be one instance where a biological invasion may have a positive outcome.

1. Brandl, S.J., Robbins, W.D., and Bellwood, D.R. (2015). Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use. Proc. R. Soc. B. 282, 20151147. 2. Chong-Seng, K.M., Nash, K.L., Bellwood, D.R., and Graham, N.A.J. (2014). Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33, 409–419. 3. Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J., Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.E., et al. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637. 4. Albins, M.A., and Hixon, M.A. (2013). Worst case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environ. Biol. Fishes 96, 1151–1157. 5. Sutherland, W.J., Clout, M., Côté, I.M., Daszak, P., Depledge, M.H., Fellman, L., Fleishman, E., Garthwaite, R., Gibbons, D.W., De Lurio, J., et al. (2010). A horizon scan of global conservation issues for 2010. Trends Ecol. Evol. 25, 1–7. 6. Sax, D.F., Stachowicz, J.J., Brown, J.H., Bruno, J.F., Dawson, M.N., Gaines, S.D., Grosberg, R.K., Hastings, A., Holt, R.D., Mayfield, M.M., et al. (2007). Ecological and evolutionary insights from species invasions. Trends Ecol. Evol. 22, 465–471. 7. Vergés, A., Steinberg, P.D., Hay, M.E., Poore, A.G.B., Campbell, A.H., Ballesteros, E., Heck, Jr., K.L., Booth, D.J., Coleman, M.A., Feary, D.A., et al. (2014). The tropicalization of temperate marine ecosystems: climatemediated changes in herbivory and community phase shifts. Proc. R. Soc. B 281, 20140846. 8. Parravicini, V., Azzurro, E., Kulbicki, M., and Belmaker, J. (2015). Niche shift can impair the ability to predict invasion risk in the marine realm: an illustration using Mediterranean fish invaders. Ecol. Lett. 18, 246–253. 9. Marras, S., Cucco, A., Antognarelli, F., Azzurro, E., Milazzo, M., Bariche, M., Butenschön, M., Kay, S., Di Bitetto, M., Quattrocchi, G., et al. (2015). Predicting future thermal habitat suitability of competing native and invasive fish species: from metabolic scope to oceanographic modelling. Conserv. Physiol. 3, cou059. 10. Floeter, S.R., Rocha, L.A., Robertson, D.R., Joyeux, J.C., Smith-Vaniz, W.F., Wirtz, P., Edwards, A.J., Barreiros, J.P., Ferreira, C.E.L., Gasparini, J.L., et al. (2008). Atlantic reef fish biogeography and evolution. J. Biogeogr. 35, 22–47.

SUPPLEMENTAL INFORMATION 1

Supplemental Information including additional discussion can be found with this article online at http://dx.doi.org/10.1016/j. cub.2016.11.018.

Current Biology 27, R1–R18, January 9, 2017

ARC Centre of Excellence for Coral Reef Studies and College of Science and Engineering, James Cook University, Townsville, QLD 4811, Australia. 2 Lead Contact. *E-mail: [email protected]