TY - JOUR
AU - Gruber, David F.
AB - Abstract Bioluminescence, the ability to produce light by living organisms, has evolved independently in numerous lineages across the tree of life. Luminous forms are found in a wide range of taxonomic groups from bacteria to vertebrates, although the great majority of bioluminescent organisms are marine taxa. Within the phylum Annelida, bioluminescence is widespread, present in at least 98 terrestrial and marine species that represent 45 genera distributed in thirteen lineages of clitellates and polychaetes. The ecological diversity of luminous annelids is unparalleled, with species occupying a great variety of habitats including both terrestrial and marine ecosystems, from coastal waters to the deep-sea, in benthic and pelagic habitats from polar to tropical regions. This great taxonomic and ecological diversity is matched by the wide array of bioluminescent colors—including yellow light, which is very rare among marine taxa—different emission wavelengths even between species of the same genus, and varying patterns, chemical reactions and kinetics. This diversity of bioluminescence colors and patterns suggests that light production in annelids might be involved in a variety of different functions, including defensive mechanisms like sacrificial lures or aposematic signals, and intraspecific communication systems. In this review, we explore the world of luminous annelids, particularly focusing on the current knowledge regarding their taxonomic and ecological diversity and discussing the putative functions and chemistries of their bioluminescent systems. Introduction The phylum Annelida, more commonly known as segmented or bristle worms, is an ancient and ecologically important lineage of Lophotrochozoans, with around 17,000 described species (Struck et al. 2011; Weigert and Bleidorn 2016). Annelids are present in a wide variety of environments ranging from terrestrial and freshwater to marine habitats, including species that are highly specialized to occupy unique ecological niches such as hydrothermal vents or whale falls (Rouse and Pleijel 2001; Struck et al. 2011; Purschke et al. 2014; Weigert and Bleidorn 2016). Subsequent adaptive radiations within Annelida have led to the remarkably high species diversity we see today and have also resulted in an extraordinary variety of body types, life strategies, feeding mechanisms and striking adaptations. One of these adaptations is bioluminescence. Bioluminescence, the ability to produce light by living organisms, is a biological property that has evolved independently in many lineages across the tree of life (Harvey 1952; Haddock et al. 2010). Bioluminescent light results from a chemical reaction involving the oxidation of a light-emitting molecule—luciferin—by a specific enzyme—luciferase (Shimomura 2012). In some organisms, the luciferin is tightly bound to luciferase and oxygen forming a photoprotein, and light production is triggered when the photoprotein binds to a co-factor (Deheyn and Latz 2009). There are several types of photoproteins based on their chemical identity and the cofactor they require. For example, in coelenterates, ctenophores, and radiolarians, calcium is required to trigger luminescence, whereas the photoproteins of the bivalve Pholas and some polychaetes seem to bind to superoxide radicals, and the millipede Motyxia requires ATP and magnesium to produce light (Shimomura 1985). It is estimated that bioluminescence has originated independently at least 40 times (Haddock et al. 2010), but the evolutionary origins of most systems remain unclear. The strong antioxidative properties of luciferin and its high reactivity with ROS (reactive oxygen species) like superoxides and peroxides (Devillers et al. 1999; Haddock et al. 2010), has led to a prominent evolutionary theory suggesting that bioluminescence first originated as a mechanism for reducing oxidative stress (Rees et al. 1998; Labas et al. 2001). Because exposure to oxidative stress is reduced in the deeper layers of the ocean, a functional shift might have occurred from its antioxidative to its light-emitting function, when marine organisms began to colonize the deep ocean and the selective pressure for antioxidative defense mechanisms was decreased (Rees et al. 1998). Bioluminescent forms are found in a wide range of taxonomic groups from bacteria to vertebrates, but despite this broad phylogenetic diversity, the great majority of light-producing organisms are marine taxa. More than 80% of the approximately 700 bioluminescent genera known to date are marine organisms (Shimomura 2012, Widder 2010). Bioluminescence is nearly absent in freshwater taxa, with the exception of the limpet Latia (Meyer-Rochow and Moore 1988; Ohmiya et al. 2005) and some insect larvae, and it is rare within terrestrial ecosystems. Fireflies are the most prominent group of bioluminescent terrestrial taxa, but there are other examples, such as the gastropod Dyakia striata (Isobe et al. 1988; Copeland and Daston 1989,), millipedes of the genus Motyxia (Marek et al. 2011), and several beetles (Wood 1995; Day et al. 2004), earthworms (Wampler and Jamieson 1979; Rota et al. 2003) and fungi (Weitz 2004; Desjardin et al. 2008; Purtov et al. 2015). However, bioluminescence in terrestrial organisms is dwarfed when compared to marine environments. In the water column, Martini and Haddock (2017) recently reported that 76% of more than 350,000 observed individuals are bioluminescent, with 93% of the identified polychaetes (∼9.8% of the total individuals examined) exhibiting bioluminescence. Light production is closely related with different vital functions such as reproduction, feeding, defense, or communication and therefore, the light produced by different luminous organisms has varying wavelengths, intensities and patterns, based on the function associated to light production and the physical properties of the environment they occupy (Morin 1983; Widder 2001; Haddock 2006). For example, in terrestrial environments bioluminescent light is generally yellow, whereas it has a green hue in shallow waters and it is usually blue in deep-sea habitats, corresponding to the wavelengths that propagate best in these environments (Haddock et al. 2010; Widder 2010). In a similar way, bioluminescent glows are thought to function as a lure or attraction signal, whether directed to prey or potential mates, whereas sudden flashes are generally associated with defensive functions, used to startle and confuse predators (Haddock et al. 2010). Within Annelids, bioluminescence has evolved independently in several lineages (Fig. 1) (Haddock et al. 2010; Shimomura 2012) possibly contributing to the high taxonomic diversity we observe today (Ellis and Oakley 2016) with almost 100 luminous species distributed in thirteen families (Fig. 1, Table 1). Their ecological diversity is also unparalleled, with species occupying a wide range of habitats including both terrestrial and marine ecosystems from coastal waters to the deep-sea, and both benthic and pelagic habitats from polar to tropical regions. Their taxonomic and ecological diversity is matched by the wide array of bioluminescent colors (Figs. 1 and 2, Table 1), including yellow light emitters which are extremely rare among marine taxa (Fig. 2E) (Widder 2010), and widely varying patterns, chemical reactions, and kinetics. We present the current state of knowledge regarding luminous annelids, particularly focusing on their taxonomic and ecological diversity and discussing the putative functions and chemistries of their bioluminescent systems. Fig. 1 Open in new tabDownload slide Distribution and spectral diversity of bioluminescence in the phylum Annelida. Lineages surrounded by ovals include bioluminescent species. Color of the oval indicates the bioluminescence emission maxima of a representative species; the corresponding wavelength, species name, and a schematic representation are shown to the right. Ovals with a dashed-line contour indicate lineages with dubious reports of bioluminescent species. Cladogram based on phylogenetic reconstruction from Weigert and Bleidorn (2016). Visible light spectrum is shown at the bottom for reference. Fig. 2 Open in new tabDownload slide Bioluminescent annelids. (A) Chaetopterus variopedatus, scale bar 2 mm; (B) Harmothoe imbricata, scale bar 2 mm; (C) Fridericia heliota bioluminescence, scale bar 1 mm; (D) Thelepus cincinnatus, scale bar 2 mm; (E) Tomopteris helgolandica photographed under natural light (left) and in the dark after KCl-induced bioluminescence (right), scale bar 500 µm; (F) Eusyllis blomstrandi, scale bar 2 mm; (G) Odontosyllis fulgurans, scale bar 2 mm; (H) Close-up of Odontosyllis enopla male, scale bar 1 mm; (I) Odontosyllis enopla female bioluminescent display, still frame from Supplementary Video S1, scale bar 2 cm. Images courtesy of Alexander Semenov (A, C), Fredrik Pleijel (B, D, F, G), Anaïd Gouveneaux (E) and John Sparks (I). Image E was adapted with permission from The Journal of Experimental Biology (Gouveneaux and Mallefet 2013). Table 1 Biochemical characteristics of annelid bioluminescence. Peak emission wavelengths and components necessary for bioluminescence reaction in luminous clitellates (top half) and polychaetes (bottom half). Shaded rows correspond to terrestrial species and clear rows indicate marine species. Bioluminescent species for which none of these characteristics are known are not included in the table. Species . λ max (nm) . Components of bioluminescence system . References . Family Acanthodrilidae  Diplocardia alba 501 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. eigeni 505 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. longa 507 Luciferin/luciferase/H2O2/O2/Cu2+ Bellisario et al. (1972)  Diplotrema heteropora 545 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Microscolex phosphoreus 538 Luciferin/luciferase/H2O2 Wampler (1982) Family Enchytraeidae  Fridericia heliota 478 Luciferin/luciferase/ATP/Mg2+/O2 Rodionova et al. (2003)  Henlea sp. 464 Luciferin/luciferase/O2/Ca2+ Rodionova et al. (2002) Family Lumbricidae  Eisenia lucens 493 Riboflavin/luciferase/aldehyde/O2 Pes et al. (2016) Family Megascolecidae  Fletcherodrilus fasciatus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  F. unicus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Pontodrilus bermudensis 540 Luciferin/luciferase/H2O2 Wampler and Jamieson (1986)  Spenceriella cormieri – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. curtisi 535 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. minor 531 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. noctiluca – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Octochaetidae  Octochaetus multiporus >570 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Flabelligeridae  Flota flabelligera 497 – Francis et al. (2016)  Poeobius meseres 495 – Francis et al. (2016) Family Chaetopteridae  Chaetopterus variopedatus 463 Riboflavin/luciferase/H2O2/Fe2+ Nicol (1957a), Rawat and Deheyn (2016) Family POLYNOIDAE  Gattyana cirrhosa 517 – Nicol (1957b)  Harmothoe longisetis 512 – Nicol (1957b)  Harmothoe extenuate 515 – Nicol (1957b)  Malmgrenia lunulata 510 Polynoidin/superoxide anions/O2 Bassot and Nicolas (1995)  Polynoe scolopendrina 511 – Nicol (1957b) Family Syllidae  Odontosyllis enopla 507 Luciferin/luciferase/Mg2+/cyanide/O2 Shimomura et al. (1963)  Odontosyllis phosphorea 494 Photoprotein/co-factor Deheyn and Latz (2009) Family Terebellidae  Polycirrus perplexus 445 Huber et al. (1989) Family Tomopteridae  Tomopteris sp. 565 Aloe-emodin/luciferase Francis et al. (2014)  Tomopteris sp. 493 – Francis et al. (2016)  T. carpenter 574 – Gouveneaux et al. (2016)  T. helgolandica 573 – Gouveneaux and Mallefet (2013)  T. nisseni 565 – Latz et al. (1988)  T. pacifica 549 – Gouveneaux et al. (2016)  T. planktonis 450 – Gouveneaux et al. (2016)  T. septentrionalis 557 – Gouveneaux et al. (2016) Species . λ max (nm) . Components of bioluminescence system . References . Family Acanthodrilidae  Diplocardia alba 501 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. eigeni 505 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. longa 507 Luciferin/luciferase/H2O2/O2/Cu2+ Bellisario et al. (1972)  Diplotrema heteropora 545 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Microscolex phosphoreus 538 Luciferin/luciferase/H2O2 Wampler (1982) Family Enchytraeidae  Fridericia heliota 478 Luciferin/luciferase/ATP/Mg2+/O2 Rodionova et al. (2003)  Henlea sp. 464 Luciferin/luciferase/O2/Ca2+ Rodionova et al. (2002) Family Lumbricidae  Eisenia lucens 493 Riboflavin/luciferase/aldehyde/O2 Pes et al. (2016) Family Megascolecidae  Fletcherodrilus fasciatus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  F. unicus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Pontodrilus bermudensis 540 Luciferin/luciferase/H2O2 Wampler and Jamieson (1986)  Spenceriella cormieri – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. curtisi 535 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. minor 531 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. noctiluca – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Octochaetidae  Octochaetus multiporus >570 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Flabelligeridae  Flota flabelligera 497 – Francis et al. (2016)  Poeobius meseres 495 – Francis et al. (2016) Family Chaetopteridae  Chaetopterus variopedatus 463 Riboflavin/luciferase/H2O2/Fe2+ Nicol (1957a), Rawat and Deheyn (2016) Family POLYNOIDAE  Gattyana cirrhosa 517 – Nicol (1957b)  Harmothoe longisetis 512 – Nicol (1957b)  Harmothoe extenuate 515 – Nicol (1957b)  Malmgrenia lunulata 510 Polynoidin/superoxide anions/O2 Bassot and Nicolas (1995)  Polynoe scolopendrina 511 – Nicol (1957b) Family Syllidae  Odontosyllis enopla 507 Luciferin/luciferase/Mg2+/cyanide/O2 Shimomura et al. (1963)  Odontosyllis phosphorea 494 Photoprotein/co-factor Deheyn and Latz (2009) Family Terebellidae  Polycirrus perplexus 445 Huber et al. (1989) Family Tomopteridae  Tomopteris sp. 565 Aloe-emodin/luciferase Francis et al. (2014)  Tomopteris sp. 493 – Francis et al. (2016)  T. carpenter 574 – Gouveneaux et al. (2016)  T. helgolandica 573 – Gouveneaux and Mallefet (2013)  T. nisseni 565 – Latz et al. (1988)  T. pacifica 549 – Gouveneaux et al. (2016)  T. planktonis 450 – Gouveneaux et al. (2016)  T. septentrionalis 557 – Gouveneaux et al. (2016) Open in new tab Table 1 Biochemical characteristics of annelid bioluminescence. Peak emission wavelengths and components necessary for bioluminescence reaction in luminous clitellates (top half) and polychaetes (bottom half). Shaded rows correspond to terrestrial species and clear rows indicate marine species. Bioluminescent species for which none of these characteristics are known are not included in the table. Species . λ max (nm) . Components of bioluminescence system . References . Family Acanthodrilidae  Diplocardia alba 501 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. eigeni 505 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. longa 507 Luciferin/luciferase/H2O2/O2/Cu2+ Bellisario et al. (1972)  Diplotrema heteropora 545 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Microscolex phosphoreus 538 Luciferin/luciferase/H2O2 Wampler (1982) Family Enchytraeidae  Fridericia heliota 478 Luciferin/luciferase/ATP/Mg2+/O2 Rodionova et al. (2003)  Henlea sp. 464 Luciferin/luciferase/O2/Ca2+ Rodionova et al. (2002) Family Lumbricidae  Eisenia lucens 493 Riboflavin/luciferase/aldehyde/O2 Pes et al. (2016) Family Megascolecidae  Fletcherodrilus fasciatus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  F. unicus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Pontodrilus bermudensis 540 Luciferin/luciferase/H2O2 Wampler and Jamieson (1986)  Spenceriella cormieri – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. curtisi 535 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. minor 531 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. noctiluca – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Octochaetidae  Octochaetus multiporus >570 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Flabelligeridae  Flota flabelligera 497 – Francis et al. (2016)  Poeobius meseres 495 – Francis et al. (2016) Family Chaetopteridae  Chaetopterus variopedatus 463 Riboflavin/luciferase/H2O2/Fe2+ Nicol (1957a), Rawat and Deheyn (2016) Family POLYNOIDAE  Gattyana cirrhosa 517 – Nicol (1957b)  Harmothoe longisetis 512 – Nicol (1957b)  Harmothoe extenuate 515 – Nicol (1957b)  Malmgrenia lunulata 510 Polynoidin/superoxide anions/O2 Bassot and Nicolas (1995)  Polynoe scolopendrina 511 – Nicol (1957b) Family Syllidae  Odontosyllis enopla 507 Luciferin/luciferase/Mg2+/cyanide/O2 Shimomura et al. (1963)  Odontosyllis phosphorea 494 Photoprotein/co-factor Deheyn and Latz (2009) Family Terebellidae  Polycirrus perplexus 445 Huber et al. (1989) Family Tomopteridae  Tomopteris sp. 565 Aloe-emodin/luciferase Francis et al. (2014)  Tomopteris sp. 493 – Francis et al. (2016)  T. carpenter 574 – Gouveneaux et al. (2016)  T. helgolandica 573 – Gouveneaux and Mallefet (2013)  T. nisseni 565 – Latz et al. (1988)  T. pacifica 549 – Gouveneaux et al. (2016)  T. planktonis 450 – Gouveneaux et al. (2016)  T. septentrionalis 557 – Gouveneaux et al. (2016) Species . λ max (nm) . Components of bioluminescence system . References . Family Acanthodrilidae  Diplocardia alba 501 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. eigeni 505 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  D. longa 507 Luciferin/luciferase/H2O2/O2/Cu2+ Bellisario et al. (1972)  Diplotrema heteropora 545 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Microscolex phosphoreus 538 Luciferin/luciferase/H2O2 Wampler (1982) Family Enchytraeidae  Fridericia heliota 478 Luciferin/luciferase/ATP/Mg2+/O2 Rodionova et al. (2003)  Henlea sp. 464 Luciferin/luciferase/O2/Ca2+ Rodionova et al. (2002) Family Lumbricidae  Eisenia lucens 493 Riboflavin/luciferase/aldehyde/O2 Pes et al. (2016) Family Megascolecidae  Fletcherodrilus fasciatus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  F. unicus – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  Pontodrilus bermudensis 540 Luciferin/luciferase/H2O2 Wampler and Jamieson (1986)  Spenceriella cormieri – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. curtisi 535 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. minor 531 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979)  S. noctiluca – Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Octochaetidae  Octochaetus multiporus >570 Luciferin/luciferase/H2O2 Wampler and Jamieson (1979) Family Flabelligeridae  Flota flabelligera 497 – Francis et al. (2016)  Poeobius meseres 495 – Francis et al. (2016) Family Chaetopteridae  Chaetopterus variopedatus 463 Riboflavin/luciferase/H2O2/Fe2+ Nicol (1957a), Rawat and Deheyn (2016) Family POLYNOIDAE  Gattyana cirrhosa 517 – Nicol (1957b)  Harmothoe longisetis 512 – Nicol (1957b)  Harmothoe extenuate 515 – Nicol (1957b)  Malmgrenia lunulata 510 Polynoidin/superoxide anions/O2 Bassot and Nicolas (1995)  Polynoe scolopendrina 511 – Nicol (1957b) Family Syllidae  Odontosyllis enopla 507 Luciferin/luciferase/Mg2+/cyanide/O2 Shimomura et al. (1963)  Odontosyllis phosphorea 494 Photoprotein/co-factor Deheyn and Latz (2009) Family Terebellidae  Polycirrus perplexus 445 Huber et al. (1989) Family Tomopteridae  Tomopteris sp. 565 Aloe-emodin/luciferase Francis et al. (2014)  Tomopteris sp. 493 – Francis et al. (2016)  T. carpenter 574 – Gouveneaux et al. (2016)  T. helgolandica 573 – Gouveneaux and Mallefet (2013)  T. nisseni 565 – Latz et al. (1988)  T. pacifica 549 – Gouveneaux et al. (2016)  T. planktonis 450 – Gouveneaux et al. (2016)  T. septentrionalis 557 – Gouveneaux et al. (2016) Open in new tab Diversity of luminous annelids: which worms glow? Approximately 98 luminous annelid species representing 45 genera have been reported so far, distributed in five clitellate families including Acanthodrilidae, Enchytraeidae, Lumbricidae, Megascolecidae, and Octochaetidae, and eight polychaete families, namely Acrocirridae, Chaetopteridae, Cirratulidae, Flabelligeridae, Polynoidae, Syllidae, Terebellidae, and Tomopteridae (Fig. 1, Table 1) (Harvey 1952; Herring 1978, 1987; Shimomura 2012). Among these, there are species that occupy an incredible variety of habitats and ecological niches and show a corresponding diversity of bioluminescent colors and patterns. In this section, we review the diversity of luminescent annelids both in terms of taxonomic and ecological diversity and provide information about their bioluminescent displays and patterns. Terrestrial taxa The only known terrestrial luminous annelids identified to date are several earthworm species in the class Clitellata. Clitellates, which include earthworms, branchiobdellids, and leeches, comprise around one-third of all annelid species currently described, and are characterized by the clitellum, a glandular epidermal structure with the shape of a ring involved in reproduction (Erséus 2005; Erséus et al. 2010). Bioluminescent clitellates are found in five families of earthworms and potworms: Acanthodrilidae, Enchytraeidae, Lumbricidae, Megascolecidae, and Octochaetidae. With few exceptions, bioluminescent clitellates secrete a luminescent coelomic fluid under mechanical, chemical or electric stimulation. The bioluminescent system is located in granules packed in cells of the secreted coelomic fluid (Wampler and Jamieson 1979, 1986; Petushkov et al. 2002, 2014; Rota et al. 2003; Pes et al. 2016). Enchytraeidae Enchytraeids or potworms are probably the most ubiquitous taxon of clitellates, with around 700 species distributed throughout the world (Erséus 2005; Erséus et al. 2010). Bioluminescent terrestrial enchytraeids are found in the genera Fridericia and Michaelseniella and usually inhabit soils rich in organic matter. The majority of luminescent enchytraeids produce flashes of light after stimulation triggers the release of a luminous coelomic slime (Wampler and Jamieson 1986; Petushkov and Rodionova 2005), with the exception of Fridericia heliota (Fig. 2C), whose bioluminescent system is located under the cuticle, in a region of epidermal glandular cells not related to coelomic cells. The luminescent granules are scattered throughout the body, being most abundant in the prostomium and pygidium (Petushkov et al. 2003, 2014; Rota et al. 2003; Petushkov and Rodionova 2007). Lumbricidae Lumbricid earthworms are essential members of the soil biota playing a major role in biogeochemical cycles (Edwards and Bohlen 1995). There are around 300 described species of lumbricids, generally characterized by the presence of a multilayered clitellum (Pérez-Losada et al. 2012). All records of bioluminescence in the Lumbricidae refer to species currently classified in Eisenia, probably limited to only two or three species, including Eisenia fetida and E. lucens (Pes et al. 2016). Luminescence in lumbricids is reported from the coelomic fluid which contains the granular coelomocytes with the luminescent compounds and is secreted through the dorsal pores in response to strong mechanical or chemical stimulation (Rota et al. 2003). Megascolecoidea The majority of luminescent clitellates belong to the earthworm superfamily Megascolecoidea, with around 30 luminous species distributed in 13 genera in the families Ancanthodrilidae, Megascolecidae, and Octochaetidae (Rota et al. 2003). Luminescence in megascolecoideans is reported after mechanical, chemical, or electrical stimulation from the coelomic fluid discharged through either the dorsal pores or the mouth and anus (Wampler and Jamieson 1979, 1986; Wampler 1982), although light production varies among species. The ubiquitous earthworm Microscolex phosphoreus has a quick bright response even upon disturbance of the surrounding soil, while in other species the response is much slower and light emission is weaker. Interestingly, in others like Digaster keasti mechanical stimulation does not elicit light production, which is only obtained after exposure to hydrogen peroxide (Harvey 1952; Jamieson 1977, Jamieson and Wampler 1979; Wampler 1982; Rota et al. 2003). Marine taxa All marine bioluminescent annelids reported to date are polychaetes, except for a handful of clitellates including the potworms Henlea and Enchytraeus (Enchytraeidae) and the earthworm Pontodrilus (Megascolecidae) which are found in different intertidal habitats (Wampler and Jamieson 1979, 1986; Healy and Coates 1999) (Table 1). The term Polychaeta refers to a paraphyletic group of annelids, characterized by having parapodia with chitinous chaetae. Despite being an artificial grouping, the term is commonly used to distinguish non-clitellate annelids from clitellates (Weigert and Bleidorn 2016). Bioluminescence in polychaetes is widespread, present in numerous species distributed in eight families including Acrocirridae, Chaetopteridae, Cirratulidae, Flabelligeridae, Polynoidae, Syllidae, Tomopteridae, and Terebellidae (Harvey 1952; Herring 1987; Haddock et al. 2010; Shimomura 2012). Light production in polychaetes is very diverse, with emission wavelengths ranging from 445 nm in Terebellidae to 573 nm in Tomopteridae (Fig. 1, Table 1) and varying patterns and kinetics, suggesting it serves many different functions. For example, Chaetopterus and swarming females of Odontosyllis show long glows emitted from secretions (Hastings and Morin 1991; Fischer and Fischer 1995; Gaston and Hall 2000; Deheyn and Latz 2009; Deheyn et al. 2013), whereas polynoids and swarming males of Odontosyllis produce flashes of light via intracellular bioluminescence (Bassot and Nicolas 1995; Fischer and Fischer 1995; Deheyn and Latz 2009; Martin and Plyuscheva 2009). Bioluminescent polychaetes are found in a wide range of marine habitats from intertidal and shallow waters to the deep-sea, both in the benthic and pelagic zones, from polar to tropical regions (Raymond and DeVries 1976; Gaston and Hall 2000; Francis et al. 2016). Pelagic taxa Acrocirridae and Flabelligeridae Acrocirridae and Flabelligeridae are sister families of cirratuliform pelagic and benthopelagic polychaetes that share several features including gelatinous sheathes, transparent bodies, and the capability to produce light (Osborn and Rouse, 2010). Luminous acrocirrids include species of the deep-sea genus Swima, which carry luminescent “bombs” that are released upon disturbance, rapidly lighting up and glowing intensely for many seconds (Osborn et al. 2009, 2011). These bioluminescent structures are in fact four pairs of modified branchiae that immediately produce green light when autotomized. Mechanical stimulation of any part of the body results in the detachment of a bomb (Osborn et al. 2011). Among the Flabelligeridae, there are also bioluminescent swimming species, such as Poeobius meseres and several species of the genus Flota which produce flashes of light as spots near the bristle junctions (Francis et al. 2016). Tomopteridae Tomopterids are dorsoventrally flattened holopelagic polychaetes mainly characterized by their modified parapodia, conspicuous palps, and long parapodial cirri on the second segment (Halanych et al. 2007). Most species are transparent or have little pigmentation and a number of them are capable of producing light. Bioluminescence in tomopterids was first reported in the parapodial rosettes (glandular organs) of Tomopteris mariana (Greeff 1882, 1885; Dales 1971). Most tomopterids produce a golden yellow bioluminescent light that is under nervous control (Fig. 2E) (Dales 1971; Latz et al. 1988; Haddock et al. 2010; Gouveneaux and Mallefet 2013) but interestingly, species that emit blue light have also been reported recently (Francis et al. 2016; Gouveneaux et al. 2016). Benthic taxa Chaetopteridae Chaetopterids are a basal branching lineage of marine, filter-feeding annelids, mainly benthic and tube-dwelling worms with the body divided in three distinct regions—anterior, middle, and posterior—(Osborn et al. 2007; Weigert et al. 2014). Two genera, Chaetopterus and Mesochaetopterus have bioluminescent representatives (Harvey 1952; Herring 1987). Bioluminescence is common among Chaetopterus species, which secrete a steadily luminous slime from various parts of the body and emit a flash of light from the posterior segments lasting a few seconds (Nicol 1952; Osborn et al. 2007; Shimomura 2012; Branchini et al. 2013; Deheyn et al. 2013). Chaetopterus variopedatus, for example (Fig. 2A), emits transitory undispersed light and secretes luminescent mucus that is scattered in the surrounding water when direct mechanical stimulation or freshwater are applied to the peristomial palps, feeding structures, dorsal surface or notopodia (Nicol 1952), while Chaetopterus gregarious produces weak bluish luminous mucus through the palps and notopodia (Nishi et al. 2000). An unusual pelagic deep-water chaetopterid, Chaetopterus pugaporcinus, emits light in two forms: it produces bright blue light around the peristomium and prostomium during 3–6 s that extinguishes abruptly, and releases minute green bioluminescent particles from the mid-dorsal ciliated groove and posterior end, that are dispersed throughout a mucous cloud and glow intensely for 1–2 s before slowly fading (Osborn et al. 2007). Cirratulidae Cirratulids typically burrow in soft sediments and have a large number of elongate filaments along the body, some of which occur as an anterior cluster of grooved tentacles for deposit feeding (Blake 1996). There are several species of bioluminescent cirratulids in the genera Caulleriella and Chaetozone whose epitokous forms (sexually mature individuals) become bioluminescent (Petersen 1999; Rouse and Pleijel 2001; Gibbs 2009). For example, sexually mature individuals of Caulleriella fragilis and also atokous (not sexually mature) specimens of Caulleriella parva produce a bluish light when disturbed (Petersen 1999). Chaetozone caputesocis has also been observed to emit a greenish light from photophores found mainly in the epidermis of abdominal segments (Gibbs 2009). There are some additional reports of bioluminescent cirratulids in the genera Cirratulus, Dodecaceria, and Tharyx (Harvey 1952; Herring 1987). Polynoidae Polynoids are the largest family of scale worms, which occur in all marine benthic habitats from the intertidal zone to the deep sea (Norlinder et al. 2012). Polynoids are characterized by a series of paired scales or elytra covering the dorsal surface of the body (Fig. 2B). Upon disturbance, some species emit flashes of light from the ventral epithelium of the scales. If the stimulus is strong, one or more glowing scales might be detached while the animal swims away (Nicol 1953; Bassot and Nicolas 1995; Shimomura 2012; Martin and Plyuscheva 2009). Bioluminescence has been reported in several species including Harmothoe imbricata (Fig. 2B), Harmothoe lunulata and Acholoe astericola. In the luminous species, the ventral epithelium of the elytra has a layer of luminescent cells or photocytes, which are modified epidermal cells not present in the non-luminous species (Nicol 1953; Martin and Plyuscheva 2009). Syllidae The family Syllidae is a highly diverse family of polychaetes present in nearly all marine benthic habitats and characterized by a specialization of the digestive tube named proventricle (Rouse and Pleijel 2001; Aguado et al. 2012). Syllids are known for their striking reproductive modes, which involve strong physical, morphological, and behavioral modifications, in some cases linked to bioluminescent displays. There are several luminescent species in the genera Odontosyllis (Fig. 2G, H, I), Eusyllis (Fig. 2F), and Pionosyllis mainly found in shallow coastal waters (Zörner and Fischer 2007; Deheyn and Latz 2009; Haddock et al. 2010). The behavioral aspects of the bioluminescence display linked to swarming and spawning in Odontosyllis have been thoroughly studied, but little is known about the molecular mechanisms or chemistry of the bioluminescent system (Galloway and Welch 1911; Potts 1913; Huntsman 1948, Markert et al. 1961; Tsuji and Hill 1983; Fischer and Fischer 1995; Gaston and Hall 2000). The first record of a bioluminescent Odontosyllis was likely by Christopher Columbus in November of 1492 when the Santa María was approaching the Bahamas (Crawshay 1935). It was first assumed that the species was the Bermudian O. enopla, but it is more likely the species was O. luminosa, later described by San Martin (1990) from Cuba (Gaston and Hall 2000). The first account of Odontosyllis reproduction and bioluminescent display comes from Galloway and Welch (1911). The authors recorded the spawning periodicity of O. enopla (Fig. 2H, I) from Bermuda, reporting its correlation with the lunar cycle and daily periodicity. In this species, females appear first at the surface showing a bright continuous glow while swimming rapidly in small circles (Fig. 2H, Supplementary Video S1). The males swim directly to the females, emitting flashes of light, and they both rotate together releasing gametes in the water column. Later authors added more information, reporting the display lasts roughly half an hour, beginning around 55 min after sunset, each month after a full moon. Females glow for 3–8 s, while males give 2–3 quick flashes of light when approaching a female (Huntsman 1948; Markert et al. 1961). The species O. octodentata from Puerto Rico and O. luminosa from Belize have similar swarming and bioluminescent displays the second night after a full moon, around 75 min and 55–65 min after sunset, respectively, more frequently during the summer months (Erdman 1965; Gaston and Hall 2000). Potts (1913) described the reproductive behavior of another bioluminescent species, O. phosphorea from British Columbia and reported its swarming periodicity, which takes place during the last quarter or beginning of first quarter of the moon, about half an hour after sunset. Tsuji and Hill (1983) studied the spawning of the same species in southern California and described its strong seasonality. The authors reported that the bioluminescent display and spawning are correlated with the monthly lunar cycles and occur shortly after sunset at fortnightly intervals from June through October, lasting around 30 min. Unlike the rest of Odontosyllis species, in O. phosphorea the first flashes of light are usually from males. The females appear shortly after, swimming in circles, flashing and secreting a bright green luminous mucus along with the gametes (Potts 1913; Tsuji and Hill 1983). Other syllids also produce light, most notably the species Eusyllis blomstrandi (Figure 2F), which has paired epidermal luminescent regions in each segment that produce light upon stimulation. Light emission is usually localized on a posterior group of segments, where it seems to be intracellular and can be turned on and off very rapidly (Zörner and Fischer 2007). Terebellidae Terebellids are tubicolous polychaetes that usually inhabit soft substrates worldwide. They are selective deposit feeders that use their numerous buccal tentacles to collect organic matter from the sea floor (Garraffoni and Lana 2008). Bioluminescence in terebellids was first described by Dahlgren (1916) when he observed the production of a bright violet-blue luminous secretion in the tip of the tentacles of Polycirrus auranticus. Harvey (1926) also reported bioluminescence as a luminous secretion in Thelepus cincinnatus (Fig. 2D). The extracellular nature of bioluminescence has also been suggested in other terebellids, including P. auranticus and P. caliendrum. However, Huber et al. (1989) argued that the extremely rapid flashes of light produced by P. perplexus in response to stimulation are inconsistent with the hypothesis that light production is extracellular and concluded that bioluminescence in this species is not secretory. Other reports There are additional, less detailed and sometimes dubious reports of bioluminescent annelids in the literature (Herring 1978, 1987). For example, the planktonic genera Alciopina and Rhynchonereella (Alciopidae) have been reported to be luminescent (Dales 1971). An unidentified species of Onuphis (Onuphidae) was reported to have pairs of lateral luminous spots in each segment that emit a bluish-green light when stimulated (Haneda 1955). A survey of bioluminescence organisms in Antarctica described the bioluminescence of Aglaophamus foliosus (Nepthydae) (Raymond and DeVries 1976) and early authors reported light production in Nereididae species including Nereis noctiluca, N. pelagica, and N. radiata (Harvey 1952). But in general, these reports are questionable as they are based in single observations in which the actual source of the light was uncertain. In addition, the identification of the species is sometimes doubtful, such as in the case of the nereid species which were probably misidentified and most likely correspond to syllids (Harvey 1952). Functions of bioluminescence in Annelida: why do worms glow? The biological significance of light production is poorly understood in most systems mainly because of the difficulty of linking bioluminescence to a specific biological or ecological function (Oba and Schultz 2014). There are a few instances in which the function of light production is well understood such as in fireflies that use flash signals for sexual communication (Lewis and Cratsley 2008) or midshipman fish and lantern sharks that use bioluminescence for camouflage through counterillumination (Claes et al. 2010; Harper and Case 1999). In other cases, the highly complex neuronally controlled light organs and light-associated behaviors (Anctil and Case 1977; Gouveneaux and Mallefet 2013) indicate bioluminescence must serve an important biological role (Oba and Schultz 2014). As a general rule in annelids, bioluminescence is poorly understood and this lack of knowledge makes it extremely difficult to link light production to a specific function. Within clitellates, for example, the diverse bioluminescent systems and chemistries displayed by different species suggest that light production might be associated to a variety of functions, yet in species that do not produce light immediately upon stimulation it is thought to be a functionless byproduct of other metabolic processes (Jamieson 1977; Oba and Schultz 2014). Despite the differences observed in the bioluminescence characteristics and light emission patterns in the different groups of luminous annelids, in most cases, light production has been associated with a defensive function (Harvey 1952, Herring 1978, Huber et al. 1989; Deheyn and Latz 2009; Osborn et al. 2009; Haddock et al. 2010; Shimomura 2012; Gouveneaux and Mallefet 2013) and in a few instances, it has been linked to intraspecific communication (Dales 1971; Harvey 1952; Latz et al. 1988; Fischer and Fischer 1995; Gaston and Hall 2000; Gouveneaux and Mallefet 2013). It is important to mention that as far as we know, there have been no published studies that provide experimental evidence to support any of the hypothesized functions of light production in annelids. The suggested functions are based on inferences from morphological and physiological characteristics and in the best-case scenario, supported by in situ behavioral observations (i.e., Gaston and Hall 2000; Zörner and Fischer 2007; Deheyn and Latz 2009). In this section, we discuss the putative functions associated with light production in annelid worms. Defense Startle mechanism Tubicolous species of Chaetopteridae and Terebellidae exude glowing particles from their tube when disturbed and it has been hypothesized that bioluminescence acts as a startle mechanism against predators and commensals (Harvey 1952; Morin 1983; Shimomura 2012). The glowing mucus of Chaetopterus has also been proposed to have a defensive function by sticking to the predator, interfering with its locomotion and making it more visible and vulnerable to its own predators (Rawat and Deheyn 2016). In Odontosyllis species (Fig. 2G and H), it is well known that bioluminescence is used for intraspecific communication during reproduction (see Section “Intraspecific communication”) but light production has also been observed in juveniles and in adults that had returned to benthic life after spawning, suggesting that it might serve additional functions (Fischer and Fischer 1995; Gaston and Hall 2000; Deheyn and Latz 2009). For example, internal bioluminescence in O. enopla has been observed during the nocturnal foraging behavior of adults and following mechanical stimulation (Fischer and Fischer 1995). Intense flashes of light have also been reported from adults and juveniles O. phosphorea after mechanical stimulation, indicating bioluminescence might be used for predator deterrence acting as a startle mechanism (Deheyn and Latz 2009). Sacrificial lure In scale worms (Polynoidae), bioluminescence has been suggested to serve as a warning or distracting mechanism (Nicol 1953; Herring 1978; Bassot and Nicolas 1995; Martin and Plyuscheva 2009; Oba et al. 2016). Polynoids emit light from the dorsal scales or elytra (Fig. 2B), which are easily autotomized in response to a strong stimulus and flash brightly from some time, acting as a sacrificial lure that allows the animal to escape (Nicol 1953; Herring 1978). A similar mechanism has been proposed to explain the function of the bioluminescent “bombs” released by the deep-sea acrocirrid Swima bombiviridis, which glow intensely for many seconds distracting the predator while the animal swims away (Osborn et al. 2009). In the syllid Eusyllis blomstrandi (Fig. 2F), a similar, albeit more extreme behavior has been observed. Light emission in this species is localized in the posterior end of the body, which upon strong stimulation becomes autotomized and glows extremely brightly for a few seconds, while the anterior non-luminescent end swims away (Zörner and Fischer 2007). The anterior end of the worm is capable of regenerating the lost segments while the posterior fragment can survive for some time, but it is unable to regenerate the head and feeding structures and thus, it might serve as a decoy or sacrificial lure attracting the attention of predators while the anterior fragment escapes (Zörner and Fischer 2007). Aposematic signal Both terebellids and chaetopterids produce short wavelength luminescence at around 440 nm, which has been suggested to function as an aposematic signal, specifically in the terebellid Polycirrus perplexus where it might indicate the distastefulness and toxicity of its tentacles (Dahlgren 1916; Morin 1983; Huber et al. 1989). Similarly, flashes of light of O. luminosa may also represent an aposematic signal indicating distastefulness or toxicity as predators have been observed to regurgitate recently ingested worms (Gaston and Hall 2000). Intraspecific communication Probably the only case in which annelid light production can be unquestionably associated with a particular function is in the courtship displays of Odontosyllis worms. Bioluminescent light is used for mate attraction, acting as a swarming cue. In most species, the females swim to the surface first and swim in circles releasing gametes and producing a steady bright green light (Fig. 2I, Supplementary Video S1) that attracts the males, which swim towards the females and also release gametes (Galloway and Welch 1911; Markert et al. 1961). Luminescence in the cirratulid Chaetozone caputesocis, has also been suggested to serve an intraspecific communication role during reproduction, to maintain cohesion during the pelagic swarming events (Petersen 1999; Gibbs 2009). In other species, light production is thought to function as a mechanism for intraspecific communication but not necessarily related to reproduction. For example, the species-specific distribution of the luminous organs and the atypical emission of yellow light in Tomopteridae has led several authors to suggest that bioluminescence provides a private communication channel (Harvey 1952; Dales 1971; Latz et al. 1988; Gouveneaux and Mallefet 2013). Because contact between planktonic organisms in the open ocean is difficult, other bioluminescent annelids with a pelagic lifestyle, such as the chaetopterid C. pugaporcinus, may also use bioluminescence as an intraspecific communication system. This hypothesis is not restricted to the open ocean, as the bioluminescent system of the terrestrial annelid Digaster keasti is thought to function as an intraspecific recognition tool (Jamieson 1977; Herring 1978). Chemistry of bioluminescent systems: how do worms glow? Although knowledge on the chemistry of annelid luminescent systems is scarce, there is a recognized wide diversity of chemical reactions and kinetics among the different species. The luminescent system of most clitellates requires luciferin, luciferase, hydrogen peroxide, oxygen, and an activator that varies among different species (Table 1) (Petushkov et al. 2002; Shimomura 2012). For example, the bioluminescence of Diplocardia longa (Megascolecidae) is triggered by copper, while in Henlea sp. (Enchytraeidae) the activator is calcium and Fridericia heliota (Enchytraeidae) requires magnesium and ATP as a co-substrate (Petushkov et al. 2002, 2003, 2014; Petushkov and Rodionova 2005). In the megascolecid earthworm Diplocardia longa the luciferin has been identified as N-isovaleryl-3-aminopropanal (Fig. 3A) and the luciferase isolated and characterized as a 300 kDa heterotrimeric copper metalloprotein (Bellisario and Cormier 1971; Bellisario et al. 1972; Ohtsuka et al. 1984; Oba et al. 2016). Bioluminescence in other megascolecoidean genera is also triggered by hydrogen peroxide and the reaction can be activated with the addition of D. longa luciferin or luciferase suggesting the chemistry of light production is equivalent (Wampler and Jamieson 1979; Wampler 1982; Oba et al. 2016). Although there is spectral and biochemical data that might support that bioluminescence in clitellates requires hydrogen peroxide, the relevant studies provided experimental evidence in vitro, and thus this hypothesis has to be considered with caution (Bellisario and Cormier 1971; Rudie et al. 1976; Wampler and Jamieson 1979, 1986). Fig. 3 Open in new tabDownload slide Chemical structures of annelid luciferins and lumazines. (A) Diplocardia longa luciferin; (B) Fridericia heliota luciferin; (C–E) Odontosyllis undecimdonta lumazines. More recently, different luminescent systems have been described in clitellates with the structural characterization of a novel luciferin in Fridericia heliota (Fig. 3B) (Petushkov et al. 2002, 2003, 2014) and studies on the bioluminescence system of the European earthworm Eisenia lucens (Pes et al. 2016). The structure of the F. heliota luciferin has an unusual modified peptidic nature and represents a novel mechanism of luminescence with the oxidation of an oxalate moiety and a fluorescent CompX moiety as the light emitter (Petushkov et al. 2014). The coelomic fluid of E. lucens has a high content of riboflavin which suggests that light production involves the oxidation of riboflavin by atmospheric oxygen (Pes et al. 2016). The chemistry of bioluminescence in parchment tubeworms has been mainly studied in Chaetopterus variopedatus (Shimomura and Johnson 1966; Anctil 1979; Martin and Anctil 1984; Zinner 1986; Shimomura 2012; Branchini et al. 2013; Deheyn et al. 2013; Rawat and Deheyn 2016). The luminous system includes a photoprotein that emits blue light in presence of hydrogen peroxide and iron and the amount of light emitted is proportional to the amount of photoprotein that reacts (Shimomura and Johnson 1966; Shimomura 2012). The luminous mucus of Chaetopterus has been recently studied in detail, suggesting that riboflavin or a structurally related derivative is the light emitter in this species and revealing that ferritin is involved in light production possibly storing iron to facilitate light production (Branchini et al. 2013; Rawat and Deheyn 2016). In scale worms, the bioluminescent system involves a membrane photoprotein of about 65 kDa called polynoidin which is specifically triggered by superoxide radicals that result from the oxidation of reduced riboflavin in the presence of calcium (Nicolas et al. 1982; Bassot 1987; Bassot and Nicolas 1995; Martin and Plyuscheva 2009). The polynoid photoprotein seems to contain a tightly bound cofactor or alternatively, it may function using its conformational change to transfer the energy from the superoxide radicals to the light emitter directly (Martin and Plyuscheva 2009). Interestingly, polynoidin is also present in non-luminescent scale worms suggesting that bioluminescence might have originated from a mechanism able to quench superoxide radicals (Martin and Plyuscheva 2009). In Syllidae, the bioluminescent systems of O. enopla and O. phosphorea have been briefly investigated. The luciferin of O. enopla has been partially purified showing that light emission requires the presence of magnesium, molecular oxygen, and crude luciferase, although its chemical structure has not yet been determined (Table 1) (Shimomura et al. 1963; Trainor 1979). More recently, analyses of the bioluminescent mucus of O. phosphorea revealed that the reaction appears to involve a photoprotein (Table 1) instead of a luciferin-luciferase reaction, therefore representing an alternative mechanism in this species (Deheyn and Latz 2009). Additionally, several lumazines and lumazine derivatives (Fig. 3C−E) have been isolated from the metabolites of the luminescent Japanese species O. undecimdonta although their connection to the bioluminescence system remains unclear (Inoue et al. 1991; Sato and Fukuya 2000; Oba et al. 2016). The light emitting substance in the bioluminescence system of the holopelagic Tomopteridae is thought to be a membrane-bound photoprotein tightly associated with small particles (Shimomura 2012; Francis et al. 2014). A recent study isolated the fluorescent yellow–orange pigment found in the luminous exudate and body of Tomopteris and identified the compound as aloe-emodin, suggesting it might act as the light emitter in Tomopteris (Francis et al. 2014). Conclusions and future prospects Numerous lineages of annelids have independently evolved a wide diversity of bioluminescence systems, making Annelida a very interesting phylum for bioluminescence research. However, annelid luminescent systems are currently poorly understood, with luciferin structures known for only two earthworm species and no luciferases or photoproteins characterized so far. Likewise, little is known regarding the biological or ecological functions of bioluminescence in annelids or the evolutionary origins of the bioluminescent systems in the different lineages. Nonetheless, the development of new instruments and technological devices like remotely operated vehicles (ROVs) and low-light underwater cameras has already led to the discovery of new bioluminescent annelids (Osborn et al. 2009) and provided important observations regarding species interactions and distribution of bioluminescent taxa (Gouveneaux et al. 2016; Phillips et al. 2016; Martini and Haddock 2017). These technologies will continue to progress and improve our understanding of the diversity and functions of bioluminescence in annelids in the future. Likewise, the recent advances in Next-Generation sequencing technologies and bioinformatics methods, as well as biochemical analytical tools will lead to an exponential increase in our knowledge on the molecular basis of bioluminescence and the chemistry of light-producing molecules. The ocean seems full of unknown, and likely novel, annelid systems that may also provide illuminating insights and opportunities for the development of new biomedical and biotechnological applications. Acknowledgments We wish to express our gratitude to John Sparks (American Museum of Natural History, USA), Fredrik Pleijel (University of Gothemburg, Sweeden), Alexander Semenov (Lomonosov Moscow State University, Russia), and Anaïd Gouvenaux (Catholic University of Louvain, Belgium) for kindly granting permission to use photographs and videos of bioluminescent annelids. We also thank Marta Novo (Universidad Nacional de Educación a Distancia, Spain) for her help with questions regarding earthworm taxonomy. Funding This work was supported by Baruch College Weissman School of Arts and Sciences, NOA OER grant #NA160AR0110198 and NSF grant #1556213 to D.F.G. and CUNY Science Scholarship to A.V. References Aguado MT , San Martín G, Siddall ME. 2012 . Systematics and evolution of syllids (Annelida, Syllidae) . Cladistics 28 : 23450 . Google Scholar Crossref Search ADS WorldCat Anctil M. 1979 . The epithelial luminescent system of Chaetopterus variopedatus . Can J Zool 57 : 1290 – 310 . Google Scholar Crossref Search ADS WorldCat Anctil M , Case JF. 1977 . The caudal luminous organs of lanternfishes: general innervation and ultrastructure . Am J Anatomy 149 : 1 – 21 . Google Scholar Crossref Search ADS WorldCat Bassot JM. 1987 . A transient intracellular coupling explains the facilitation of responses in the bioluminescent system of scale worms . J Cell Biol 105 : 2235 – 43 . Google Scholar Crossref Search ADS PubMed WorldCat Bassot JM , Nicolas MT. 1995 . 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Google Scholar Crossref Search ADS WorldCat Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2017. This work is written by US Government employees and is in the public domain in the US. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2017. This work is written by US Government employees and is in the public domain in the US.
TI - Glowing Worms: Biological, Chemical, and Functional Diversity of Bioluminescent Annelids
JF - Integrative and Comparative Biology
DO - 10.1093/icb/icx017
DA - 2017-07-01
UR - https://www.deepdyve.com/lp/oxford-university-press/glowing-worms-biological-chemical-and-functional-diversity-of-MACoZg0x1f
SP - 18
EP - 32
VL - 57
IS - 1
DP - DeepDyve
ER -