- Email: [email protected]
Cryptobenthic reef fishes
Current Biology
Magazine ghostly white carbonate chimneys up to 60 m tall that are permeated by thick, snotty biofilms of bacteria and archaea (Figure 1). The metabolic strategies of organisms living in hot, highly alkaline (pH 10–11) water rich in hydrogen and methane are currently being studied. Water venting from Lost City chimneys never exceeds ~100ºC, meaning that life is permitted throughout the hydrothermal system. Animals at the Lost City are very small but biologically diverse, and one mussel species observed on the chimneys hosts two distinct kinds of endosymbiotic bacteria, one powered by hydrogen or hydrogen sulfide and the other by methane. Did life originate in hydrothermal vents? Many different lines of evidence point to a role for hydrothermal vents in the early evolution of life. Deepsea hydrothermal vents would have provided a constant habitat sheltered from catastrophic events that most likely rendered Earth’s surface inhospitable at various points in its early history. Therefore, even if life originated on the surface, deep-sea vents would have been a crucial refuge in times of heavy asteroid bombardment or other surface crises. Furthermore, many elements required for life, such as metal co-factors of essential enzymes, are only found in large concentrations near hydrothermal vents. Hydrothermal minerals are capable of catalyzing, in the absence of enzymes, at least some steps of carbon-fixation pathways. Experimental simulations of hydrothermal chimneys have demonstrated polymerization of DNA molecules. Moreover, the thermal gradients of ~50–100ºC across the highly porous Lost City chimneys, in particular, would have provided favorable conditions for many simultaneous chemical reactions in separate microchambers, which could have led to the synthesis of the first organic molecules on Earth. The inorganic compartments of hydrothermal chimneys have also been proposed as the scaffolding on which the first cell membranes could have been formed. Therefore, even if one is unconvinced that life could have arisen de novo in a hydrothermal chimney, these environments must have played important roles in the early evolution of biochemistry thanks to the rich diversity of chemical reactions and physical compartments that they host. R452
What have hydrothermal vents taught us about possible extraterrestrial life? They have shown that the availability of sunlight may not be the most important factor when searching for life on other planets. Instead, the most important requirement for life may be a geologically active planet, manifested in the form of plate tectonics and magmatic activity that can support hydrothermal circulation. The recent discovery of the Lost City hydrothermal field raises the question of whether serpentinization reactions could even support the origin and evolution of life without any additional geological activity. If so, then life may require only some liquid water and the right kind of rock. Interestingly, rocks capable of serpentinization are found on most, if not all, rocky bodies in our solar system. This possibility notwithstanding, our present understanding of hydrothermal vent ecosystems inspires a view of life’s origin as an emergence from global geological and geochemical processes, rather than as an accident caused by a fortuitous spark in an isolated pond. Mars, Europa (moon of Jupiter) and Enceladus (moon of Saturn) are currently being explored as places where hydrothermal systems could have been active in the past and perhaps remain active today.
Quick guide
Cryptobenthic reef fishes Christopher H.R. Goatley1,* and Simon J. Brandl2 What are cryptobenthic reef fishes? On reefs around the world, fishes display a remarkable abundance and diversity of shapes and colours. However, perhaps even more remarkable is that most casual observers on reefs probably do not see half of the fishes that live there. This ‘hidden half’ of the fish community is comprised of cryptobenthic reef fishes — adult fishes typically less than 5 cm long that are visually or behaviourally cryptic, and live near to or even within the seabed (Figure 1). Cryptobenthic reef fish communities can be comprised of many species and families, but perhaps the most common and widespread members are the gobies (family Gobiidae) and the blenny-like fishes (suborder Blennioidei). While small camouflaged fishes may not sound particularly exciting at first, cryptobenthic reef fishes display extraordinary diversity and are of critical ecological importance on reefs worldwide.
Where can I find out more? Dubilier, N., Bergin, C., and Lott, C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725–740. Kelley, D.S., Baross, J.A., and Delaney, J.R. (2002). Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu. Rev. Earth Planet. Sci. 30, 385–491. Kreysing, M., Keil, L., Lanzmich, S., and Braun, D. (2015). Heat flux across an open pore enables the continuous replication and selection of oligonucleotides towards increasing length. Nat. Chem. 7, 203–208. Martin, W., Baross, J., Kelley, D., and Russell, M.J. (2008). Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814. Russell, M.J., and Martin, W. (2004). The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29, 358–363. Schrenk, M.O., Huber, J.A., and Edwards, K.J. (2010). Microbial provinces in the subseafloor. Annu. Rev. Mar. Sci. 2, 279. Stüeken, E.E., Anderson, R.E., Bowman, J.S., Brazelton, W.J., Colangelo–Lillis, J., Goldman, A.D., Som, S.M., and Baross, J.A. (2013). Did life originate from a global chemical reactor? Geobiology 11, 101–126. Van Dover, C.L., German, C.R., Speer, K.G., Parson, L.M., and Vrijenhoek, R.C. (2002). Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295, 1253–1257.
Department of Biology, University of Utah, Salt Lake City, USA. E-mail: [email protected]
Current Biology 27, R431–R510, June 5, 2017 © 2017 Elsevier Ltd.
What do cryptobenthic reef fishes do? In short, cryptobenthic reef fishes live fast and die young. For most of them, growth, reproduction and death happen at extraordinary rates. After settlement on the reef, often in a very specific microhabitat, adult fishes spend most of their time feasting on microscopic prey, such as small invertebrates (e.g. copepods), filamentous algae, coral mucus or detritus. Most of the energy gained from feeding is used for growth, which lets cryptobenthic reef fishes grow rapidly throughout their lives. The remaining time and energy is spent largely on a surprising variety of different social and reproductive strategies, including sex changes, territoriality, and both monogamous and polygamous reproduction. Some species, like the dwarf goby Eviota sigillata, can produce 7.4 generations per year, which results in a steady stream of new recruits of cryptobenthic fishes to the reef. After a few weeks, it’s all over. In fact, with a maximum age of just 59 days in the wild,
Current Biology
Magazine
Figure 1. Cryptobenthic reef fish diversity. Cryptobenthic fishes from the Caribbean (left panel, photographed in photo-tanks) and Indo-Pacific (right panels, photographed in situ). Phototank species (top to bottom): Scartella cristata (Blenniidae), Starksia weigti (Labrisomidae), Acanthemblemaria aspera (Chaenopsidae), Lythrypnus okapia (Gobiidae), Labrisomus guppyi (Labrisomidae), Lucayablennius zingaro (Chaenopsidae), Priolepis hipoliti (Gobiidae). In situ species (top row, left–right): Eviota pellucida (Gobiidae), Enneapterygius atrogulare (Tripterygiidae), Nemateleotris magnifica (Microdesmidae), (middle row, all from the Gobiidae) Paragobiodon xanthosoma, Trimma lantana, Amblyeleotris wheeleri, (bottom row) Eviota prasites (Gobiidae), Ecsenius stictus (Blenniidae), Luposicya lupus (Gobiidae). Photos by R.M. Bonaldo, S.J. Brandl, J.M. Casey, C.H.R. Goatley and J.P. Krajewski.
E. sigillata currently holds the record for the shortest lifespan of all vertebrates, and the goby Coryphopterus kuna is the only known fish that has a larval stage that lasts longer than its adult lifespan. Where are cryptobenthic fishes found? Everywhere! Wherever researchers have used specific techniques to look for cryptobenthic reef fishes — usually involving anaesthetising all fishes within a small area — they have found them to be surprisingly abundant. This has been the case for studies conducted on tropical, subtropical and temperate reefs throughout the Indo-Pacific, Caribbean, Gulf of California, Mediterranean and Atlantic. In almost every habitat, in every sea, fish communities are numerically dominated by these small cryptic fishes. While communities of cryptobenthic fishes are found almost everywhere, individual
species of cryptobenthic reef fishes can be very picky about where they live. For example, coral gobies (genera including Gobiodon, Luposicya and Pleurosicya) are often dependent upon single species of coral for shelter. While these are extreme examples, most other cryptobenthic reef fishes have some specific habitat requirements. These needs, combined with the complexity of reef habitats, lead to cryptobenthic fish communities being highly variable among reefs. The community composition of cryptobenthic reef fishes is also affected by depth. Recent work has begun to highlight that cryptobenthic reef fish communities are not restricted to shallow reefs, and many species are only found in deeper waters. In fact, sampling of deep reefs in the Caribbean using manned submersibles in depths of 300 m or more continues to yield
a plethora of new species. Keeping in mind that sampling tiny fishes in a complex but dimly lit environment using a manned submersible is like searching for a needle in a haystack in a dark barn using a forklift, we will probably continue to find new cryptobenthic reef fish species on deep-water reefs from locations worldwide. In addition, new species from shallow reefs are described regularly, studies that sample cryptobenthic reef fishes with appropriate methods are still geographically patchy and cryptobenthic fish species generally have small geographic ranges. All of this suggests that we are probably grossly underestimating the biodiversity of cryptobenthic fishes worldwide. How many cryptobenthic fishes are there? Lots. On tropical reefs around the world, the average abundance of
Current Biology 27, R431–R510, June 5, 2017
R453
Current Biology
Magazine cryptobenthic reef fishes is frequently around ten individuals per square meter, and in rubble beds of the Great Barrier Reef there are often more than 20 individuals per square meter. This makes cryptobenthic reef fishes by far the most abundant group of vertebrates on reefs. Similarly, their diversity is unrivalled by any other marine vertebrate. Shallow lagoons of the Great Barrier Reef often harbour more than ten species per square meter. In particular, the gobies (Gobiidae), which often dominate cryptobenthic reef fish communities, consist of more species than any other family of fishes. It is likely that the extreme diversity of cryptobenthic reef fishes, along with ecological differences among species, helps to ensure the (more or less) peaceful coexistence of these densely populated communities. Why should we care about cryptobenthic fishes? Beyond their visual appeal (Figure 1), their fast paced lifestyles make cryptobenthic reef fishes a vital part of coral reef food webs. Incredibly, up to 8% of the population of cryptobenthic reef fishes are eaten every day, and almost any fish capable of catching and eating cryptobenthic reef fishes will readily do so. In other words, by growing quickly and steadily replenishing their populations, cryptobenthic reef fishes transfer energy from their microscopic prey into more accessible food (fish tissue) for larger predators. Thus, cryptobenthic reef fishes are a fundamental part of complex coral-reef food webs, helping to support large reef fishes and coastal populations that depend on these fish stocks. Cryptobenthic fishes also offer scientists precious insights into the process of evolution in the world’s oceans. While populations of many marine species are connected across vast areas of ocean through the dispersal of planktonic larvae, the short lifespans of cryptobenthic fishes mean that they often do not move very far, and populations are easily isolated from one another. Combined with short generation times, this isolation appears to have led to the relatively rapid formation of new species. A good example are dwarf gobies (Eviota spp.), many of which have evolved relatively recently (within the last halfmillion years) from common ancestors. Now, each species occupies specific regions or microhabitats. Finally, despite R454
their abundance and short life-cycles, the highly specific needs of cryptobenthic reef fishes mean they are often the first species to succumb to environmental changes. Thus, cryptobenthic reef fishes may serve as sensitive indicators of the impacts of disturbances on coral reefs, allowing the identification of threats and an increased window of opportunity for management responses to be applied. What next for cryptobenthic reef fish research? We still have much to learn about these tiny, but fascinating, animals. Most importantly, the actual number of species and individuals of cryptobenthic reef fishes and their ecological role is unknown in most locations. Better ways of sampling cryptobenthic reef fishes (such as UV-fluorescence surveys or standardized habitat modules) may be useful. These would permit direct comparisons of cryptobenthic fish communities from different locations and facilitate their exploration in areas that are difficult to access. Where can I find out more? Ackerman, J.L., and Bellwood, D.R. (2000). Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 206, 227–237. Bellwood, D.R., Hoey, A.S., Ackerman, J.L., and Depczynski, M. (2006). Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob. Change Biol. 12, 1587–1594. Depczynski, M., and Bellwood, D.R. (2003). The role of cryptobenthic reef fishes in coral reef trophodynamics. Mar. Ecol. Prog. Ser. 256, 183–191. Depczynski, M., and Bellwood, D.R. (2006). Extremes, plasticity, and invariance in vertebrate life history traits: insights from coral reef fishes. Ecology 87, 3119–3127. Smith-Vaniz, W.F., Jelks, H.L., and Rocha, L.A. (2006). Relevance of cryptic fishes in biodiversity assessments: a case study at Buck Island Reef National Monument, St. Croix. Bull. Mar. Sci. 79, 17–48. Tornabene, L., Ahmadia, G.N., Berumen, M.L., Smith, D.J., Jompa, J., and Pezold, F. (2013). Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota). Mol. Phyl. Evol. 66, 391–400. Tornabene, L., Van Tassell, J.L., Robertson, D.R., and Baldwin, C.C. (2016). Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs. Mol. Ecol. 25, 3662–3682. Willis, T.J., and Anderson, M.J. (2003). Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar. Ecol. Prog. Ser. 257, 209–221. 1 Function, Evolution and Anatomy Research Lab, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia. 2Tennenbaum Marine Observatories Network, Smithsonian Institution, Edgewater, MD 21037, USA. *E-mail: [email protected]
Current Biology 27, R431–R510, June 5, 2017 © 2017 Elsevier Ltd.
Primer
Polar oceans in a changing climate David K.A. Barnes* and Geraint A. Tarling Most of Earth’s surface is blue or white, but how much of each would depend on the time of observation. Our planet has been through phases of snowball (all frozen), greenhouse (all liquid seas) and icehouse (frozen and liquid). Even during current icehouse conditions, the extent of ice versus water has changed considerably between ice ages and interglacial periods. Water has been vital for life on Earth and has driven and been influenced by transitions between greenhouse and icehouse. However, neither the possession of water nor having liquid and frozen seas are unique to Earth (Figure 1). Frozen water oceans on the moons Enceladus and Europa (and possibly others) and the liquid and frozen hydrocarbon oceans on Titan probably represent the most likely areas to find extraterrestrial life. We know very little about life in Earth’s polar oceans, yet they are the engine of the thermohaline ‘conveyorbelt’, driving global circulation of heat, oxygen, carbon and nutrients as well as setting sea level through change in ice-mass balance. In regions of polar seas, where surface water is particularly cold and dense, it sinks to generate a tropic-ward flow on the ocean floor of the Pacific, Atlantic and Indian Oceans. Cold water holds more gas, so this sinking water exports O2 and nutrients, thereby supporting life in the deep sea, as well as soaking up CO2 from the atmosphere. Water from mid-depths at lower latitudes flows in to replace the sinking polar surface water. This brings heat. The poles are cold because they receive the least energy from the sun, and this extreme light climate varies on many different time scales. To us, the current warm, interglacial conditions seem normal, yet such phases have represented only ~10% of Homo sapiens’ existence. Variations in Earth’s orbit (so called ‘Milankovitch cycles’) have driven cyclical alternation of glaciations (ice ages) and warmer interglacials. Despite this, Earth’s polar regions have been our planet’s most
Magazine ghostly white carbonate chimneys up to 60 m tall that are permeated by thick, snotty biofilms of bacteria and archaea (Figure 1). The metabolic strategies of organisms living in hot, highly alkaline (pH 10–11) water rich in hydrogen and methane are currently being studied. Water venting from Lost City chimneys never exceeds ~100ºC, meaning that life is permitted throughout the hydrothermal system. Animals at the Lost City are very small but biologically diverse, and one mussel species observed on the chimneys hosts two distinct kinds of endosymbiotic bacteria, one powered by hydrogen or hydrogen sulfide and the other by methane. Did life originate in hydrothermal vents? Many different lines of evidence point to a role for hydrothermal vents in the early evolution of life. Deepsea hydrothermal vents would have provided a constant habitat sheltered from catastrophic events that most likely rendered Earth’s surface inhospitable at various points in its early history. Therefore, even if life originated on the surface, deep-sea vents would have been a crucial refuge in times of heavy asteroid bombardment or other surface crises. Furthermore, many elements required for life, such as metal co-factors of essential enzymes, are only found in large concentrations near hydrothermal vents. Hydrothermal minerals are capable of catalyzing, in the absence of enzymes, at least some steps of carbon-fixation pathways. Experimental simulations of hydrothermal chimneys have demonstrated polymerization of DNA molecules. Moreover, the thermal gradients of ~50–100ºC across the highly porous Lost City chimneys, in particular, would have provided favorable conditions for many simultaneous chemical reactions in separate microchambers, which could have led to the synthesis of the first organic molecules on Earth. The inorganic compartments of hydrothermal chimneys have also been proposed as the scaffolding on which the first cell membranes could have been formed. Therefore, even if one is unconvinced that life could have arisen de novo in a hydrothermal chimney, these environments must have played important roles in the early evolution of biochemistry thanks to the rich diversity of chemical reactions and physical compartments that they host. R452
What have hydrothermal vents taught us about possible extraterrestrial life? They have shown that the availability of sunlight may not be the most important factor when searching for life on other planets. Instead, the most important requirement for life may be a geologically active planet, manifested in the form of plate tectonics and magmatic activity that can support hydrothermal circulation. The recent discovery of the Lost City hydrothermal field raises the question of whether serpentinization reactions could even support the origin and evolution of life without any additional geological activity. If so, then life may require only some liquid water and the right kind of rock. Interestingly, rocks capable of serpentinization are found on most, if not all, rocky bodies in our solar system. This possibility notwithstanding, our present understanding of hydrothermal vent ecosystems inspires a view of life’s origin as an emergence from global geological and geochemical processes, rather than as an accident caused by a fortuitous spark in an isolated pond. Mars, Europa (moon of Jupiter) and Enceladus (moon of Saturn) are currently being explored as places where hydrothermal systems could have been active in the past and perhaps remain active today.
Quick guide
Cryptobenthic reef fishes Christopher H.R. Goatley1,* and Simon J. Brandl2 What are cryptobenthic reef fishes? On reefs around the world, fishes display a remarkable abundance and diversity of shapes and colours. However, perhaps even more remarkable is that most casual observers on reefs probably do not see half of the fishes that live there. This ‘hidden half’ of the fish community is comprised of cryptobenthic reef fishes — adult fishes typically less than 5 cm long that are visually or behaviourally cryptic, and live near to or even within the seabed (Figure 1). Cryptobenthic reef fish communities can be comprised of many species and families, but perhaps the most common and widespread members are the gobies (family Gobiidae) and the blenny-like fishes (suborder Blennioidei). While small camouflaged fishes may not sound particularly exciting at first, cryptobenthic reef fishes display extraordinary diversity and are of critical ecological importance on reefs worldwide.
Where can I find out more? Dubilier, N., Bergin, C., and Lott, C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725–740. Kelley, D.S., Baross, J.A., and Delaney, J.R. (2002). Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu. Rev. Earth Planet. Sci. 30, 385–491. Kreysing, M., Keil, L., Lanzmich, S., and Braun, D. (2015). Heat flux across an open pore enables the continuous replication and selection of oligonucleotides towards increasing length. Nat. Chem. 7, 203–208. Martin, W., Baross, J., Kelley, D., and Russell, M.J. (2008). Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814. Russell, M.J., and Martin, W. (2004). The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29, 358–363. Schrenk, M.O., Huber, J.A., and Edwards, K.J. (2010). Microbial provinces in the subseafloor. Annu. Rev. Mar. Sci. 2, 279. Stüeken, E.E., Anderson, R.E., Bowman, J.S., Brazelton, W.J., Colangelo–Lillis, J., Goldman, A.D., Som, S.M., and Baross, J.A. (2013). Did life originate from a global chemical reactor? Geobiology 11, 101–126. Van Dover, C.L., German, C.R., Speer, K.G., Parson, L.M., and Vrijenhoek, R.C. (2002). Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295, 1253–1257.
Department of Biology, University of Utah, Salt Lake City, USA. E-mail: [email protected]
Current Biology 27, R431–R510, June 5, 2017 © 2017 Elsevier Ltd.
What do cryptobenthic reef fishes do? In short, cryptobenthic reef fishes live fast and die young. For most of them, growth, reproduction and death happen at extraordinary rates. After settlement on the reef, often in a very specific microhabitat, adult fishes spend most of their time feasting on microscopic prey, such as small invertebrates (e.g. copepods), filamentous algae, coral mucus or detritus. Most of the energy gained from feeding is used for growth, which lets cryptobenthic reef fishes grow rapidly throughout their lives. The remaining time and energy is spent largely on a surprising variety of different social and reproductive strategies, including sex changes, territoriality, and both monogamous and polygamous reproduction. Some species, like the dwarf goby Eviota sigillata, can produce 7.4 generations per year, which results in a steady stream of new recruits of cryptobenthic fishes to the reef. After a few weeks, it’s all over. In fact, with a maximum age of just 59 days in the wild,
Current Biology
Magazine
Figure 1. Cryptobenthic reef fish diversity. Cryptobenthic fishes from the Caribbean (left panel, photographed in photo-tanks) and Indo-Pacific (right panels, photographed in situ). Phototank species (top to bottom): Scartella cristata (Blenniidae), Starksia weigti (Labrisomidae), Acanthemblemaria aspera (Chaenopsidae), Lythrypnus okapia (Gobiidae), Labrisomus guppyi (Labrisomidae), Lucayablennius zingaro (Chaenopsidae), Priolepis hipoliti (Gobiidae). In situ species (top row, left–right): Eviota pellucida (Gobiidae), Enneapterygius atrogulare (Tripterygiidae), Nemateleotris magnifica (Microdesmidae), (middle row, all from the Gobiidae) Paragobiodon xanthosoma, Trimma lantana, Amblyeleotris wheeleri, (bottom row) Eviota prasites (Gobiidae), Ecsenius stictus (Blenniidae), Luposicya lupus (Gobiidae). Photos by R.M. Bonaldo, S.J. Brandl, J.M. Casey, C.H.R. Goatley and J.P. Krajewski.
E. sigillata currently holds the record for the shortest lifespan of all vertebrates, and the goby Coryphopterus kuna is the only known fish that has a larval stage that lasts longer than its adult lifespan. Where are cryptobenthic fishes found? Everywhere! Wherever researchers have used specific techniques to look for cryptobenthic reef fishes — usually involving anaesthetising all fishes within a small area — they have found them to be surprisingly abundant. This has been the case for studies conducted on tropical, subtropical and temperate reefs throughout the Indo-Pacific, Caribbean, Gulf of California, Mediterranean and Atlantic. In almost every habitat, in every sea, fish communities are numerically dominated by these small cryptic fishes. While communities of cryptobenthic fishes are found almost everywhere, individual
species of cryptobenthic reef fishes can be very picky about where they live. For example, coral gobies (genera including Gobiodon, Luposicya and Pleurosicya) are often dependent upon single species of coral for shelter. While these are extreme examples, most other cryptobenthic reef fishes have some specific habitat requirements. These needs, combined with the complexity of reef habitats, lead to cryptobenthic fish communities being highly variable among reefs. The community composition of cryptobenthic reef fishes is also affected by depth. Recent work has begun to highlight that cryptobenthic reef fish communities are not restricted to shallow reefs, and many species are only found in deeper waters. In fact, sampling of deep reefs in the Caribbean using manned submersibles in depths of 300 m or more continues to yield
a plethora of new species. Keeping in mind that sampling tiny fishes in a complex but dimly lit environment using a manned submersible is like searching for a needle in a haystack in a dark barn using a forklift, we will probably continue to find new cryptobenthic reef fish species on deep-water reefs from locations worldwide. In addition, new species from shallow reefs are described regularly, studies that sample cryptobenthic reef fishes with appropriate methods are still geographically patchy and cryptobenthic fish species generally have small geographic ranges. All of this suggests that we are probably grossly underestimating the biodiversity of cryptobenthic fishes worldwide. How many cryptobenthic fishes are there? Lots. On tropical reefs around the world, the average abundance of
Current Biology 27, R431–R510, June 5, 2017
R453
Current Biology
Magazine cryptobenthic reef fishes is frequently around ten individuals per square meter, and in rubble beds of the Great Barrier Reef there are often more than 20 individuals per square meter. This makes cryptobenthic reef fishes by far the most abundant group of vertebrates on reefs. Similarly, their diversity is unrivalled by any other marine vertebrate. Shallow lagoons of the Great Barrier Reef often harbour more than ten species per square meter. In particular, the gobies (Gobiidae), which often dominate cryptobenthic reef fish communities, consist of more species than any other family of fishes. It is likely that the extreme diversity of cryptobenthic reef fishes, along with ecological differences among species, helps to ensure the (more or less) peaceful coexistence of these densely populated communities. Why should we care about cryptobenthic fishes? Beyond their visual appeal (Figure 1), their fast paced lifestyles make cryptobenthic reef fishes a vital part of coral reef food webs. Incredibly, up to 8% of the population of cryptobenthic reef fishes are eaten every day, and almost any fish capable of catching and eating cryptobenthic reef fishes will readily do so. In other words, by growing quickly and steadily replenishing their populations, cryptobenthic reef fishes transfer energy from their microscopic prey into more accessible food (fish tissue) for larger predators. Thus, cryptobenthic reef fishes are a fundamental part of complex coral-reef food webs, helping to support large reef fishes and coastal populations that depend on these fish stocks. Cryptobenthic fishes also offer scientists precious insights into the process of evolution in the world’s oceans. While populations of many marine species are connected across vast areas of ocean through the dispersal of planktonic larvae, the short lifespans of cryptobenthic fishes mean that they often do not move very far, and populations are easily isolated from one another. Combined with short generation times, this isolation appears to have led to the relatively rapid formation of new species. A good example are dwarf gobies (Eviota spp.), many of which have evolved relatively recently (within the last halfmillion years) from common ancestors. Now, each species occupies specific regions or microhabitats. Finally, despite R454
their abundance and short life-cycles, the highly specific needs of cryptobenthic reef fishes mean they are often the first species to succumb to environmental changes. Thus, cryptobenthic reef fishes may serve as sensitive indicators of the impacts of disturbances on coral reefs, allowing the identification of threats and an increased window of opportunity for management responses to be applied. What next for cryptobenthic reef fish research? We still have much to learn about these tiny, but fascinating, animals. Most importantly, the actual number of species and individuals of cryptobenthic reef fishes and their ecological role is unknown in most locations. Better ways of sampling cryptobenthic reef fishes (such as UV-fluorescence surveys or standardized habitat modules) may be useful. These would permit direct comparisons of cryptobenthic fish communities from different locations and facilitate their exploration in areas that are difficult to access. Where can I find out more? Ackerman, J.L., and Bellwood, D.R. (2000). Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 206, 227–237. Bellwood, D.R., Hoey, A.S., Ackerman, J.L., and Depczynski, M. (2006). Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob. Change Biol. 12, 1587–1594. Depczynski, M., and Bellwood, D.R. (2003). The role of cryptobenthic reef fishes in coral reef trophodynamics. Mar. Ecol. Prog. Ser. 256, 183–191. Depczynski, M., and Bellwood, D.R. (2006). Extremes, plasticity, and invariance in vertebrate life history traits: insights from coral reef fishes. Ecology 87, 3119–3127. Smith-Vaniz, W.F., Jelks, H.L., and Rocha, L.A. (2006). Relevance of cryptic fishes in biodiversity assessments: a case study at Buck Island Reef National Monument, St. Croix. Bull. Mar. Sci. 79, 17–48. Tornabene, L., Ahmadia, G.N., Berumen, M.L., Smith, D.J., Jompa, J., and Pezold, F. (2013). Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota). Mol. Phyl. Evol. 66, 391–400. Tornabene, L., Van Tassell, J.L., Robertson, D.R., and Baldwin, C.C. (2016). Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs. Mol. Ecol. 25, 3662–3682. Willis, T.J., and Anderson, M.J. (2003). Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar. Ecol. Prog. Ser. 257, 209–221. 1 Function, Evolution and Anatomy Research Lab, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia. 2Tennenbaum Marine Observatories Network, Smithsonian Institution, Edgewater, MD 21037, USA. *E-mail: [email protected]
Current Biology 27, R431–R510, June 5, 2017 © 2017 Elsevier Ltd.
Primer
Polar oceans in a changing climate David K.A. Barnes* and Geraint A. Tarling Most of Earth’s surface is blue or white, but how much of each would depend on the time of observation. Our planet has been through phases of snowball (all frozen), greenhouse (all liquid seas) and icehouse (frozen and liquid). Even during current icehouse conditions, the extent of ice versus water has changed considerably between ice ages and interglacial periods. Water has been vital for life on Earth and has driven and been influenced by transitions between greenhouse and icehouse. However, neither the possession of water nor having liquid and frozen seas are unique to Earth (Figure 1). Frozen water oceans on the moons Enceladus and Europa (and possibly others) and the liquid and frozen hydrocarbon oceans on Titan probably represent the most likely areas to find extraterrestrial life. We know very little about life in Earth’s polar oceans, yet they are the engine of the thermohaline ‘conveyorbelt’, driving global circulation of heat, oxygen, carbon and nutrients as well as setting sea level through change in ice-mass balance. In regions of polar seas, where surface water is particularly cold and dense, it sinks to generate a tropic-ward flow on the ocean floor of the Pacific, Atlantic and Indian Oceans. Cold water holds more gas, so this sinking water exports O2 and nutrients, thereby supporting life in the deep sea, as well as soaking up CO2 from the atmosphere. Water from mid-depths at lower latitudes flows in to replace the sinking polar surface water. This brings heat. The poles are cold because they receive the least energy from the sun, and this extreme light climate varies on many different time scales. To us, the current warm, interglacial conditions seem normal, yet such phases have represented only ~10% of Homo sapiens’ existence. Variations in Earth’s orbit (so called ‘Milankovitch cycles’) have driven cyclical alternation of glaciations (ice ages) and warmer interglacials. Despite this, Earth’s polar regions have been our planet’s most