BULLETIN OF MARINE SCIENCE, 33(4): 787-817, 1983

COASTAL BIOLUMINESCENCE: PATTERNS AND FUNCTIONS

James G, Morin

ABSTRACT Individual bioluminescent organisms in coastal waters often occur in high densities, but the number of luminescent species is relatively low, about I to 2%. Simple emitting systems, involving either photocytes or photosecretion, tend to be the dominant luminescent types in coastal organisms, However, complex light organs, as either glandular light organs or pho- tophores, occur among some of the fishes. This situation contrasts with oceanic regions where organisms with photophores tend to dominate. Most of the luminescent signals in coastal waters occur in response to contact stimulation as simple conspicuous fast flashes «2 sec) or slow glows (> 5 sec). I suggest that most coastal luminescence functions to deter potential predation primarily by fast flashes, which repel a predator, or by slow glows, which attract a predator toward the decoy light and away from the prey. As a third anti predatory strategy, some fishes with glandular light organs produce a concealing luminescence so that their predators fail to detect them as prey. As a second major function, particularly among coastal fishes with glandular light organs, luminescence is used to obtain prey through attraction and/or detection. Thirdly, light may also be used for communication between con specifics, particularly for mating, aggregating and territorial purposes. Finally, luminescence might serve mutualistic (advertising) purposes as, for ex- ample, between luminous bacteria and visual consumers. The preponderance of simple luminescent systems present in comparatively few species in the photically complex and heterogeneous environments of coastal waters contrasts sharply with the majority of species in the more homogeneous photic environment of the mid waters of the open sea where photophores and complicated luminescent patterns dominate. Con- versely, the complex photic regimen of the shallow oceans and terrestrial environments suggests distinct parallels might exist between communications using luminescence and those using ambient reflected light, which is characteristic of all other visual communication.

The eerie luminescence emanating from breakers crashing on a beach at night has fascinated mankind for centuries. This light represents but one of a myriad ofluminous displays that can be observed in coastal waters throughout the world. While only a small proportion of coastal marine species have the capacity to bioluminesce, there are often enormous numbers of individual organisms within a small area that emit light in a variety of patterns. The photic environment of the coastal marine realm is highly complex and variable. Light levels span many orders of magnitude with depth, with time, and within the spatial complexity of the various habitats that exist along marine coasts. This variable photic regimen and the rich spatial heterogeneity of coastal regions have undoubtedly influenced the types and degree of bioluminescent development among nearshore organisms. It is not surprising, for instance, that strictly diurnal benthic and demersal organisms, which are active only during high light levels, show no tendency toward light emission. Maximum bioluminescent intensities have been determined to be over 10-1 J,tWcm-2 (Young et al., 1980) which is about 6 log units less than bright daylight at the sea surface (Clarke and Denton, 1962; Lythgoe, 1979). (As a rule, daylight attenuates about r log unit with every 100 m depth in the clearest oceanic waters.) In clear shallow waters luminescence simply is not bright enough to be detected during the day. However, light levels at the sea surface drop below 10-3 J,tWcm-2 on moonless nights (Clarke, 1968), which is well within the range where luminescence can be detected by organisms

787 788 BULLETIN OF MARINE SCIENCE, VOL. 33, NO.4. 1983 above background light. Hence, nocturnally active or nocturnally vulnerable or- ganisms could be expected to include bioluminescence in the repertoire of ad- aptations. Indeed, it is within these groups of organisms that we often find light emission as a central component in their overall activity patterns. I review three major aspects ofluminescence in coastal waters: dominance and taxonomic diversity, spatial and temporal display patterns, and the possible behavioral functions of light-emitted signals. Some obvious trends exist in the distribution, form and patterns that have been observed in shallow marine or- ganisms, particularly when compared to oceanic or terrestrial forms. These trends suggest something about the overall functions of these signals and how they relate to the life of the emitting organisms that exist in a rich ambient photic environ- ment. Environmental light has almost certainly had profound effects on the ways that luminescence has evolved in shallow seas where dim to bright light conditions, but rarely total darkness, prevail. Ways seem to have evolved that integrate luminescence into this background illumination. To provide a conceptual frame- work I present a catalogue of the potential behavioral functions of coastallumi- nescence. I start with the major categories of defense, offense and communication; examine their various subcategories; and add advertisement as a fourth major category. I show where there are data that fit into these various overlapping and non-mutually exclusive categories. This new synthesis leads to the conclusion that the majority ofluminescence seen in coastal waters is aimed at deterring potential predators. Where other functions occur, the signals are apparently displayed in such a way that predators are also effectively thwarted from using these signals to locate or capture the prey.

DOMINANT GROUPS AND DIVERSITY OF COASTAL LUMINESCENT ORGANISMS A wide variety of coastal organisms produce light. These include representatives from at least 12 phyla. In coastal environments bioluminescence is particularly common among the bacteria, dinoflagellates, cnidarians, ctenophores, annelids, crustaceans, ophiuroids, larvaceans and fishes. On the other hand, only a small fraction of the shallow water species are bioluminescent (Table 1). Worldwide, probably only 1 to 2% of all coastal species, both neritic (coastal pelagic) and benthic, produce light. For instance, using the animal data from Table I, but omitting the unspecified number of "aschelminths," ostracods and copepods, the upper limit of coastal animals along the California coast that are known to be luminescent is in the neighborhood of2.1 % (48 out of2,313 species). By including these three other groups the number would probably drop to 1 to 1.5%. I have done a similar calculation for the Woods Hole region of Massachusetts, but only for the invertebrates, and arrive at a figure of about 2.5% maximum (21 out of 802). These data serve to indicate that the number of luminescent species in coastal situations is low. In addition, there are no known luminescent plants, either aquatic or terrestrial; there are only 7 or 8 luminescent marine bacteria species known; and within the protists, many of the dinoflagellates and some of the radiolarian sarcodines produce light. The low number of coastal luminescent species contrasts with midwater organisms where luminescence is known in up to 75% of the species and 97% of the individuals of fishes (Herring and Morin, 1978), and in up to 79% of the species and 86% of the individuals of shrimps (Herring, 1976). However, in coastal waters the densities ofluminescent individ- uals can be ~xceptionally high (Table 2) and, in almost any coastal area of the world at night, luminescent displays are evident and obvious. MORIN: COASTAL BIOLUMINESCENCE 789

Dinoflagellates are major contributors to neritic and demersal bioluminescence in many parts of the world (Tett and Kelly, 1973; Kelly and Tett, 1978). The ubiquitous fairy-like scintillations observed around objects or organisms in the shallow seas are usually the result of contact stimulation with dinoflagellates. Often reefs, kelp, fishes and other objects at night underwater can be detected simply by the twinkling patterns around each of them. This luminescence is abundant enough that sea lions and other nocturnally foraging predators might use these displays to locate their prey (Hobson, 1966). Densities of dinoflagellates need not be high under these circumstances, probably less than 100 cells per liter (c/l). To get an idea of dinoflagellate densities in shallow waters, Kelly (1968) sampled the water column in Woods Hole Harbor throughout an entire year and found densities that varied from 20 to 5,000 cll, usually with at least 200 cll. The percent ofluminescent individuals in these samples varied between 20 to 85; and 70% of the dinoflagellate species tested (16 out of 23) were luminescent. Dino- flagellate numbers, either luminescent or non-luminescent, will occasionally be- come much higher during red tide blooms (Sweeney, 1979). These blooms occur in patches in coastal areas, particularly in areas of upwelling, and usually involve populations of single species. Densities may reach 3 X 107 cll (Seliger et aI., 1970). The major luminescent contributors to red tides are species of Gonyaulax, Py- rodinium. and Noctiluca. These are the forms that produce the glow seen in breakers on beaches at night. Luminous bacteria are a ubiquitous and an occasionally conspicuous component of the shallow water luminescent environment. As isolated solitary cells they cannot be seen, and may not even be luminous, but may be very bright when they occur in high numbers in fecal pellets, on decaying organics, as enteric bacteria, as parasites or as light organ symbionts of other organisms (Nealson and Hastings, 1979). The percentage ofluminous colony forming units (CFUs) cultured from various marine samples varies depending on the source. Obviously this ratio provides only the upper limit ofluminescent forms since the majority of the other bacteria in a sample will not grow on the media used (Sieburth, 1979). However, as a general rule, between 0.1 and I% of the bacteria cultured from a coastal seawater sample are luminous (O'Brien and Sizemore, 1979; Ruby and Nealson, 1978; Ruby et al., 1980; Yetinson and Shilo, 1979). The numbers of luminous colonies vary from 0.1 to almost 40 cells/ml for coastal seawater and 1.6 to 1,300 cellslg for sediments (Ruby and Nealson, 1978; O'Brien and Sizemore, 1979). The numbers fall off to about 10-3 to 10-1 cellslml in surface oceanic waters (Ruby et al., 1980). Most of the luminous bacteria (I) from tropical to subtropical nearshore surface waters are Photobacterium leiognathi and Vibrio harveyi, (2) from temperate waters are V. fischeri and V. harveyi, (3) from boreal and arctic waters are V. logei and P. phosphoreum, while (4) deep, cold oceanic waters are the almost exclusive realm of P. phosphoreum (Ruby and Nealson, 1978; Ruby and Morin, 1978; Ruby et al., 1980; Nealson and Hastings, 1979; O'Brien and Sizemore, 1979; Bang et a1., 1978; Dunlap and Morin unpublished). Luminous bacteria are related to terrestrial enteric bacteria (Nealson and Hastings, 1979) and, in the sea, their highest concentrations occur within the gut, light organ or hemocoel of other organisms. In the intestines of many fishes and crustaceans the num ber of luminous cells can be as high as 105 to 107 per ml of gut fluid and represent up to 100% of the CFU s, but is generally around 30% (Ruby and Morin, 1979). Inoculated feces may be a major pathway for dispersal utilized by these forms (Robison et a1., 1977; Nealson and Hastings, 1979; see below). Bacterial densities in light organs may exceed 1010 per ml (for review see Herring and Morin, 1978; Nealson and Hastings, 1979). 790 BULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983

Table I. Proportion of luminous animal species from benthic and neritic habitats along the. California coast*

Approx. # Known to Have Approx. # Luminescent Luminescent Species Category Species t Species * % Luminous (worldwide) § PORIFERA 70 0 0 +?B CNIDARIA Hydrozoa 80 10 13 +BNPD Anthozoa Octocorallia 18 6 33 +BD Hexacorallia 42 2 5 +BD Scyphozoa 9 0 0 +NP CTENOPHORA 8 8 100 +NP PLATYHELMINTHES 34 0 0 NEMERTEA 24 0 0 +B ASCHELMINTH COMPLEX 100's 0 0 ANNELIDA Oligochaeta 22 )? 4 +T Polychaeta 290 13 4 +BNPD SIPUNCULA 9 0 0 ECHIURA 2 0 0 ARTHROPODA Crustacea Cephalocarida and Branchiopoda few 0 0 Ostracoda dozens I 3 +BNPD Copepoda 100's 0 0 +NP Cirripedia 36 0 0 Malacostraca Mysidacea 5 0 0 +P Cumacea 7 0 0 Isopoda and Tanaidacea 110 0 0 Amphipoda 265 0 0 +NP Euphausiacea 0 0 0 +NP Decapoda 97 0 0 +NP Insecta 50 0 0 +T Diplopoda and Chilopoda 0 0 0 +T Chelicerata 41 0 0 +0 MOLLUSCA Monoplacophora and Aplacophora 0 0 0 Scaphopoda 4 0 0 Polyplacophora 30 0 0 Cephalopoda 7 0 0 +BP Gastropoda 280 0 0 +BP Bivalvia 95 0 0 +B BRYOZOAandENTOPROCTA 95 0 0 +?B PHORONIDA 8 0 0 BRACHIOPODA 4 0 0 ECHINODERMATA Echinoidea 13 0 0 Holothuroidea 18 0 0 +DP Crinoidea I 0 0 +0 Stelleroidea Asteroidea 18 0 0 +0 Ophiuroidea 16 2 13 +BD HEMICHORDATA 9 0 0 +B CHORDATA Urochordata Ascideacea 47 0 0 MORIN: COASTAL BIOLUMINESCENCE 791

Table I. Continued

Approx. # Known to Have Approx. # Luminescent Luminescen1 Species Category Species t Species * % Luminous (worldwide) § Thaliacea 5 1 20 +NP Larvaeea 2 1 50 +NP Cephalochordata 1 0 0 Venebrata Agnatha 3 0 0 Chondrichthyes 43 0 0 +PD Osteichthyes 395 3 1 +BNPD • Habitat limits were taken as the intertidal to depths of about 200 m. t Taken primarily from Smith and Carlton (1975). Morris et al. (1980) and Miller and Lea (1972). * Taken primarily from Herring (1978a), Herring and Morin (1978), and personal observations. § + = luminescent species known from: B = shallow benthic locations «200 m), D = deep benthic locations (> 200 m), N = coastal pelagiC (neritic) locations « 200 m), P ~ oceanic pelagic locations, as defined by Young (1983), T; terrestrial, ? = uncertam validity, - = no known luminescent species.

Many members of the gelatinous zooplankton in neritic waters are luminescent and abundant. These include hydromedusans, scyphomedusans, siphonophores, ctenophores and larvaceans (Table 2), The larvacean Oikopleura contributes up to nine or ten times its own individual numbers to the luminescent potential in the water column by virtue of its regularly cast off gelatinous houses that are capable of emitting flashes of light when stimulated (Galt, 1978). This, along with periodic high densities of over 104Iarvaceans/m3, produce a realized luminescent potential density of up to 105 light sources/m3. Under these conditions they probably represent an important luminescent component in many neritic com- munities (Galt, 1978). Seasonal or periodic blooms ofluminescent hydro medusae (e.g., Aequorea in the sounds of the northeast Pacific where densities reach several dozen/m3) and ctenophores (e,g., Mnemiopsis in the estuaries and bays of the northwest Atlantic where densities may exceed several hundred/m3) further in- dicate the potential importance of luminescent gelatinous zooplankton to the communities of neritic waters. Bioluminescence among benthic organisms is particularly prevalent in some of the sessile colonial cnidarians, the nocturnal suspension feeding ophiuroids, and a few tubicolous and errant polychaetes (Table 2). Within the benthic cnidarians one of the most common hydroids, Obelia (and many other campanularians), which fouls hard substrates and kelp, is remarkably luminescent. In many tem- perate locations, campanularian densities can effectively occupy the total space 2 on large (several m ) kelp fronds or dock pilings. They are often short-lived epibiotic colonies with many thousands of polyps. There may be as many as 10 to 20 uprights/cm2 and each upright will have 6 to 20 polyps and hundreds of photocytes. Most of the sand dwelling octocorals (the pennatulaceans [sea pens]) produce brilliant displays of luminescence when stimulated. They are often the dominant suspension feeding organisms on open sand or mud flats at all depths. Densities of over 100/m2 are known for Acanthoptilum in Southern California (personal observation) and up to 30 colonies/m2 for Ptilosarcus in Puget Sound (Birkeland, 1974). Some gorgon ian octocorals, zoanthid anemones, and antipa- tharians (black corals), particularly below depths of 30 m, also have the ability to emit light. Densities of these rock-dwelling luminescent organisms are generally low (lor 2/m2 maximum), but individual colony sizes may exceed 3 m in diameter for some of the black corals (personal observation). Luminescent ophiuroids are essentially sessile and primarily nocturnal suspen- sion feeders that hide in the reef or sand by day and extend their arms into the 792 IlULLETIN OF MARINE SCIENCE, VOL)3, NO, 4,1983

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"0 genus Vargula (=Cypridina) a similar complicated display pattern occurs shortly after sunset but on a very regular basis throughout the year. Densities within these aggregations may reach many dozen/m3 (Morin and Ber- mingham, 1980; Morin, unpublished). A group of demersal luminescent species are the fishes. Most occur in the tropics or in deep water (Morin, 1981). They are generally nocturnal or dim-light active, or are nocturnally or crepuscularly vulnerable. Most produce diffuse light from bacterial or gut associated glandular light organs rather than from discrete pho- tophores (for review see Morin, 1981). Ventrally expressed glandular light organs occur most commonly among the leiognathids (pony fishes), apogonids (cardinal fishes), pempherids (sweepers) and, in deep water, the macrourids (rat tails). However, some, such as the anomalopids (flashlight fishes) and monocentrids (pine-cone fishes), have cephalic glandular light organs. Discrete photophores occur in Porichthys (midshipman). Some luminescent cephalopods, cope pods, amphipods, euphausiids and carid- eans occur in neritic and nearshore demersal habitats, but they are predominantly oceanic groups and are not included here (but see Table I).

CHARACTERISTICS OF LUMINESCENCE IN COASTAL ORGANISMS The cellular basis of bioluminescence and its spatial positioning show wide variations among coastal organisms (Table 2). Light emitting structures can be grouped into simple systems, which show no development of secondary accessory structures, and light organs, complex systems which show varying combinations of pigments, reflectors, diffusers and lenses. Simple systems include photocytes, in which light is emitted from intracellular sources, and photo secretory cells, in which light is emitted extracellularly. For complex systems there appears to be confusion in the literature over the usage and definition of the terms light organ and photophore. All photophores are usually considered to be light organs, but the reverse does not necessarily hold. To clarify these terms, below I define two categories of light organs: glandular light organs and photophores. While some 798 BULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983 overlap or intergrades may exist, most light organs, particularly within the fishes, crustaceans and squids, fit naturally into one or the other of these definitions. Photocytes and, to a lesser extent, photosecretory cells are the dominant types of photoemitters in most coastal organisms (Table 2). For instance, of the lu- minescent organisms indicated in Table I, 81% emit light from photocytes, 13% by photosecretion, 2% from glandular light organs and 4% from photophores. The temporal and spectral qualities of the luminescence show some distinct patterns among coastal organisms. Most emit their light in response to an external me- chanical disturbance. The resultant display occurs either in the form of one or more flashes of less than 2 sec duration each, or as a long glow of 5 sec to more than a minute (Table 2). Bacteria emit light continuously without any external stimulation. Most fishes, crustaceans and squids have complex control mecha- nisms. The color of the light is most often green or blue-green for benthic forms, but blue to green for demersal, neritic or secretory forms (Table 2).

Photocytes Simple luminescent cells (photocytes) appear to emit bursts of light from in- tracellular sources primarily in response to contact stimulation. Spontaneous emis- sion appears to be rare. Most photocytes in metazoans appear to be modified epithelial cells that are under neural or neuroid control. Some show complex cytoplasmic architecture while others do not (for review see Sweeney, 1980). Most of these systems seem to be under tight control at the level of the cellular and subcellular membranes, presumably through direct or indirect gating of cofactor ions (e.g., Ca2+or H+, etc.) of the luminescent reaction, or through control of some molecule (e.g., 02) necessary for the luminescent reaction (for review see Case and Strause, 1978). Photocytes occur within the cnidarians, ctenophores, larvaceans, polynoids, syllids, ophiuroids, gastropods, nemerteans and several lesser studied coastal in- vertebrate groups (Table 2). Dinoflagellates and bacteria are also considered here to be unicellular photocytes. In many metazoans, photocytes usually occur in loose or tight clusters positioned in precise, highly visible anatomical locations in the most exposed or vulnerable portions of the organism. These regions include the parapodial modifications of polynoid and syllid polychaetes, the body surface of nemerteans, the bell margin of hydromedusae and some of the nectophores, gonozooids and gastrozooids of siphonophores. Vital areas are not luminescent (e.g., the cephalic regions of polynoids, syllids, nemerteans and gastropods and the disc of ophiuroids), but rather luminescence is located in places that can be lost or damaged without death to the entire organism (e.g., the elytra of poly no ids, the arms of ophiuroids or within the serially repeating units of anthozoan and hydrozoan colonies). Many photocyte-bearing organisms are relatively transparent (e.g., medusae, siphonophores, hydro polyp and anthozoan colonies, ctenophores, thaliaceans, larvaceans, dinoflagellates) or very small (dinoflagellates) so that the luminescence forms broadly radiating pulses of light projected away from the point of contact. Particularly among the benthic sessile or sedentary suspension feeders that main- tain their feeding apparatus in the water column and passively feed in the currents (hydropolyp and anthozoan colonies, ophiuroids), luminescent photocytes emit their flashes partially in all directions, but primarily into the prevailing water current, and hence toward the likely point of first contact with organisms moving with this water flow (see Morin, 1976 for pennatulaceans). Many of these systems are known to be inhibited by daylight so that they only MORIN: COASTAL BIOLUMINESCENCE 799 luminesce at night (e.g., ctenophores, dinoflagellates, hydrozoans, anthozoans; Harvey, 1926). The spectrum of the emission, blue-green to green (Table 2), is similar to the maximum wavelengths for light penetration in many coastal waters and most organisms with visual capabilities in coastal waters have pigments which can detect these wavelengths (Lythgoe, 1979; Hobson et al., 1981). The net effect of these spatial and temporal characteristics ofphotocyte emitters is that the light is expressed as a clear nocturnal signal that is (a) brief and intermittent, (b) simple, (c) bright, (d) conspicuous and in maximum contrast with the dark surrounding environment, (e) predictable, (f) oriented from the point of stimulation, (g) proportional to the stimulus intensity (shows spatial and temporal facilitation and/or summation) and (h) similar between several taxa. A few groups (the polynoid and syllid polychaetes and the ophiuroids) show an abrupt change in the signal from the flash response to a long bright glow when the luminescent photocytes and their surrounding tissues are autotomized from the remaining part of the animal, which remains dark (Brehm, 1977; Herrera, 1979; personal observation).

Photosecretory Cells These are glandular cells situated within epidermal tissues and which secrete their contents externally into the surrounding sea water (Table 2). The secretion is either produced as a surface slime (hemichordates, and also terrestrial oligo- chaetes), ejected into the flow stream of actively filtering organisms (bivalves, chaetopterid polychaetes), or left behind by nocturnally active demersal species (ostracods, syllid polychaetes). The chemical components may be packaged in different secretory cells, which then produce light as the secretions mix in the water (Harvey, 1952; Bonhomme, 1954; Bassot, 1966; Anctil, 1979a). In the benthic forms, copious clouds or strings of luminescence, which may glow for many seconds, are produced by contact stimulation. In contrast, the demersally active secretors often produce light in complex displays, often as glowing spots lasting several seconds or flashes, which is under tight circadian and circalunar control. Photosecretions occur in various dimensions, from a mm or so in diameter in some ostracod displays to many cm across in chaetopterid clouds, and they last from 5 sec up to several minutes; some can be exceedingly bright. A few luminescent secretors also seem to be able to produce short flashes ofIight under some circumstances (e.g., chaetopterids: Anctil, 1981; syllids: Hunts- man, 1948; ostracods: personal observations; hemichordates: Baxter and Pickens, 1964). The spectrum of the secreted light is usually blue or blue-green and is distinctly bluer than the light produced by most photocyte, glandular light organ and photophore emitters in coastal waters (Table 2). For stimulus induced photo secretions, the overall effect is a signal that is (a) of long duration, (b) simple, (c) bright, (d) conspicuous and in maximum contrast to the dark surroundings, (e) projected away from the dark emitter, (f) often proportional to the stimulus intensity and (g) similar across several different taxa. Glowing autotomized sections of the body in photocyte emitters (mentioned above) also show these same characteristics.

Glandular Light Organs I define glandular light organs as (I) gland-like outpocketings ofthe gut or body surface that (2) contain the light emitting materials that are either bacteria or intrinsic substances, (3) are usually surrounded by reflectors and pigments as well 800 BULLETI!' OF MARINE SCIENCE. VOL. 33. NO.4. 1983 as diffusers and/or lenses, (4) are relatively large (compared to other emitters) and (5) are few in number (usually one or two and occasionally three) in each organism. They usually produce a diffuse light. Glandular light organs occur within the fishes, especially demersal forms, and some squids and shrimps. In addition, these forms have well-developed eyes and complex behavior. Among the luminescent demersal fishes, most produce light by means of glan- dular light organs, while relatively few use photophores (Morin, 1981). Glandular light organs are primarily associated with the gut in most fishes, but there are a few spectacular examples with cephalic light organs (Table 2). In coastal waters gut-associated glandular light organs occur principally among the perciform fishes and may be bacterial (leiognathid fishes), intrinsic (pempherid fishes) or either (apogonid fishes). In all cases the light is indirectly expressed ventrally as a diffuse glow, but may, in some situations, also be distinctly displayed from the lateral or anterior surfaces in the leiognathids (Herring and Morin, 1978; Haneda, 1980; McFall-Ngai and Dunlap, 1983; Morin, 1981). Bacterial light organs are the dominant type of glandular light organ, especially in luminescent coastal demersal fishes (leiognathids, apogonids), deep-sea demersal fishes (primarily among the gadiforms) and some demersal squids (sepioids) (Herring and Morin, 1978; Her- ring et al., 1981; Herring, 1982). Species with light organs that produce light intrinsically (pempherids and some apogonids) presumably derive the luciferin for the reaction from their diet since the luciferin is chemically identical to that found in luminescent ostracods; these ostracods have been found in their gut contents; and the light organs connect to the gut (Tsuji and Haneda, 1966; Haneda, 1980; for review see also Cormier, 1978; Herring and Morin, 1978; Herring, 1982; Hastings, in press; Morin, 1981). Among the coastal demersal beryciform fishes, cephalic glandular light organs occur below each eye in the Anomalopidae (flash- light fishes) and in the lower jaw in the Monocentridae (pine-cone fishes). They are always paired and are of the bacterial type (Herring and Morin, 1978; Herring, 1982). An analogous projected cephalic luminescence occurs from discrete patches in the opercular region of leiognathids (McFall-Ngai and Dunlap, 1983). The expression of light from the light organs of these demersal fishes is com- plicated and variable. Light emission may be controlled at the level ofthe chemical components (neurally or hormonally) in the intrinsic types, or by secondary struc- tures such as shutters, windows and/or chromatophores in both the bacterial and intrinsic types (Haneda and Tsuji, 1976; Herring and Morin, 1978; Haneda, 1980; Morin, 1981). The complex organization and multiple levels of physiological control allow these organisms plasticity to manipulate the light in diverse spatial and temporal ways. The light can be projected directionally (anomalopids, mono- centrids, leiognathids) or diffusely ventral (leiognathids, pempherids, apogonids); rapidly (less than 50 msec for anomalopids) to continuously (probably all of them); and from various parts of the body (leiognathids) and in various directions (leio- gnathids and Anomalops). The light appears to be blue-green (Table 2), which is comparable to the spectral sensitivity of most visual organisms in these habitats (Lythgoe, 1979; Hobson et al., 1981).

Photophores Photophores are distinct from glandular light organs and, as a general rule, they (1) may occur anywhere on the surface of an organism, (2) are intrinsic, (3) are under neural or hormonal control, (4) are surrounded by pigments, reflectors, lenses and sometimes diffusers, (5) are relatively small (compared to glandular light organs) and (6) are numerous (dozens to hundreds) in each organism. They usually produce discrete, not diffuse, sources oflight. They occur principally within MORIN: COASTAL BIOLUMINESCENCE 801 the crustaceans, squids and fishes, especially in the mesopelagic zone (Young, 1983). All of these animals have well-developed eyes and complex behavior. The chemistry of bioluminescence varies among the different groups that possess pho- tophores (Hastings, 1983; in press), but it is not bacterial. In coastal waters only a few fishes possess discrete photophores (Table 2); these are the well-studied New World batrachoidids (toad fishes) and a few poorly-studied species of west Pacific sciaenids (croakers) and engraulids (anchovies). In all cases the photophores are numerous along the ventral and lateral surfaces of the fish (for review see Herring and Morin, 1978; Morin, 1981; Herring, 1982). The photophores of the batrachoidid Porichthys are apparently under catechol- aminergic control from the sympathetic nervous system; they produce light either as a pulsing glow or continuously (Baguet and Case, 1971; Anctil and Case, 1976; Anctil, 1979b) and may derive their luciferin from the diet (Tsuji et aI., 1972; Warner and Case, 1980). The color of the luminescence is blue-green (Table 2).

FUNCTIONS OF BIOLUMINESCENCE IN COASTAL ORGANISMS The theme among coastal luminescent organisms of fast flashes or slow glows that occur in direct response to contact stimulation and are produced from rather simply designed photoemitters would suggest that there may be a common un- derlying function. The dominant function is almost certainly to deter potential predators. In fact, antipredation is probably a common feature of most lumines- cent systems: luminescence has evolved either as a direct means of reducing predation or, where other functions are involved, as a secondary means of avoiding predation. Potentially, luminescence can be used for a number of non-mutually exclusive functions; the four main ones being (Table 3): (1) for evading or deterring predators, (2) for obtaining prey, (3) for intraspecific communication (Morin et aI., 1975) and (4) for advertisement. Other general perspectives on the functions ofluminescence can be found in the works of Buck (1978), Hastings (1976), Lloyd (1977), Tett and Kelly (1973) and Tsuji (1982).

Predator Evasion Luminescence must reside within the potential prey species for it to be useful as an anti-predatory agent. In most cases one would also expect that the predator would be able to detect and react to the signal. There are five fundamentally different, but non-exclusive, ways that the signal could operate (Table 3): (1) to repel the aggressor away from the prey (startle or frighten effect), (2) to temporarily blind the aggressor (flash bulb effect), (3) to attract the aggressor away from the prey (decoy effect), (4) to attract a predator of the aggressor to the point of contact and therefore remove the aggressor by a second order predatory event or threat thereof (burglar alarm effect) or (5) to prevent the aggressor from detecting the prey (camouflage effect). Startle Effect or Contact Flash Predator Deterrent. - Probably the most frequent- ly encountered function of luminescence in shallow water is the repelling of potential predators by using flashes of light. I call this the Contact Flash Predator Deterrent Hypothesis which assumes that a flash of light, produced upon contact by a potential predator with the luminescent prey, will deter or repel the aggressor from further pursuit and thus reduce the probability of damage or death to the potential prey. The ubiquity and similar overall design and pattern of the pho- tocyte-flash system among coastal organisms (Table 2) suggest that this is a widely used tactic. The basic message of the flash signal may be to either delay (startle) 802 BULLETIN OF MARINE SCIENCE. VOL. 33. NO.4, 1983

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*<1l U I::: <1l U > - ..<: LLJ <1l IX c::I IX o Q.. f- < Z o ~ LLJ f- IX c::I Q.. o MORIN: COASTAL BIOLUMINESCENCE 803 the predator so that the potential prey can take protective measures (e.g., con- tracting or fleeing) and/or to alert the predator that to persist will prove to be unprofitable. In addition to a general startle, an alerting signal could work in one or more overlapping ways (Table 3). First, the signal could be an aposematic warning to the aggressor that the signaling organism is potentially dangerous by virtue of unpalatability or retaliatory weaponry (see e.g., terebellids: Dahlgren, 1916; pennatulaceans: Morin, 1976; dinoflagellates: Porter and Porter, 1979). Second, rather than danger, the signal could indicate that it is futile to continue the attack since the prey item is completely or partially invulnerable. In this case no damage would necessarily be done to the predator if it persisted, rather the predator would lose foraging time and energy that might have been better spent elsewhere. Third, the signal could be a bluff, mimicking either the aposematic or invulnerability signal (Batesian mimicry). Fourth, there could be a direct effect of impairing the dark adapted photoreceptive capacity (i.e., temporarily blinding) of the aggressor; the flash-bulb effect. Finally, the signal could bring the altercation to the attention of other organisms, particularly predators of the aggressor, who might then move toward the point of contact and remove the aggressor by a second order predatory event: the indirect burglar alarm effect (Burkenroad, 1943; see below). In situations where one or more of these five defenses is involved with the luminescent flash, one would expect that a potential predator would hesitate or flee from the area of contact and forage elsewhere. In general, such a startle response seems common among any motile organisms when they are confronted by a sudden, high intensity, local stimulus to any sensory system, be it a loud noise, chemical spray or bright flash of light; i.e., discretion is the better part of valor (Edmunds, 1974; Curio, 1976). On the other hand, such stimuli often have an attractive influence on organisms at some distance from the point of contact (Sokolov, 1960); the flash calls attention to the event so that predatory organisms might well cue in on repeated brief flashes to help locate prey (Hobson et a1., 1981). It is also clear that aposematism in general is a subset of a larger category which I termed alerting signal. From this perspective for instance, a brightly colored (aposematic) diurnal organism need not necessarily be distasteful or dangerous for anti-predatory information to be intended by the color, but rather the mere fact that it is unprofitable to attack-i.e., the prey could be essentially invulnerable (Lindroth, 1971; Young, 1971; Baker and Parker, 1979). Since the contact flash signal from photocytes seems to be a rather general and also widely distributed phenomenon, it might be thought of as a rather large mimicry complex utilized by many taxa and consisting of mostly Mullerian but some Batesian mimics. Subsets involving specific colors and/or spatial and temporal patterns probably have evolved. Another feature of a luminescent contact flash is that (a) it can be relatively non-specific, i.e., the aggressor mayor may not be a predator which specifically preys on the emitter, but rather is an organism which can potentially damage the emitter either deliberately or accidentally and (b) it allows the emitter to be visually cryptic (hidden by darkness) except during the period of contact when the prey produces its alerting signal and then immediately reverts into crypsis, thus making its relocation on the part of the startled aggressor more difficult (flash and freeze effect). Such °a signal could function to alert the predator analogously to the commonly used alarm calls (Woodland et a1., 1980) and white ruinp patches (Smythe, 1970) found in many birds and mammals. Furthermore, since the lu- minescent flash occurs nearly simultaneously with the initial assault, the repellent effect, no matter what the mechanism, could be a startle reflex that would serve 804 BULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983 both to reduce the degree of damage during the initial attack and to decrease the likelihood of subsequent strikes. In pyrosomes, ctenophores, some hydromedusans and most benthic species external contact not only induces a bioluminescent flash or flashes but also pro- duces defensive motor reactions including body or polyp contraction and ciliary cessation (Baxter and Pickens, 1964; Morin, 1974; 1976; Mackie and Bone, 1978; Labas, 1980). This combination, therefore, probably further protects these animals not only by producing the alerting effect on the aggressor but also by increasing the probability of separation and protection from the aggressor. Within the py- rosomes and ctenophores other individuals also respond to a contact flash pro- duced by a conspecific by producing their own imitative emission and motor defense; presumably this response also reduces the possibility of damage to them (Mackie and Bone, 1978; Labas, 1980). While the emitting system for a wide variety of coastal organisms seems to be ideally adapted for this kind of contact flash predator deterrence, only a few studies have been done that directly address the hypothesis. First identifying the potential aggressors involved in these nocturnal interactions is difficult, in part because they probably involve organisms which normally do not feed on the emitter or do not do so with any high degree offrequency. Many organisms could be potential aggressors but, for the signal to be effective, the aggressor must be nocturnally active, visually orienting and motile. They must be organisms that come into contact with the emitter but are probably foraging for other more available prey and periodically encounter an emitter during the course of their normal nocturnal foraging activities. The interactions last for only a very brief period of time (probably less than a second or two) and they occur under extremely low light level conditions so that witnessing the event and what goes on within it is difficult. Evidence of occasional non-specific predation exists in nearly all groups of lu- minescent organisms: e.g., regenerating elytra are a common occurrence among the polynoids and so are regenerating arms among the ophiuroids and sections from pennatulaceans (personal observation). But the actual source of the predatory attack and the relative frequency are unknown. Within coastal waters the most prominent potential aggressors are the crustaceans, fishes and cephalopods. All three groups have numerous members with well-developed visual capabilities that forage widely in the water column and along the bottom. Another feature of their activities is that they have many members that are active primarily at night. For instance, on most open sand bottoms throughout the world the numbers of active crustaceans and fishes are dramatically higher at night than in the day (Morin, unpublished), often by several orders of magnitude. This applies equally for the large benthic foraging crabs, shrimps and fishes and also for the demersal fishes and small planktonic crustaceans such as isopods and amphipods (Alldredge and King, 1977; Porter and Porter, 1977; Hobson and Chess, 1976). In most cases there is little information on the frequency of flashing of lumi- nescent organisms in situ and even less about the types and frequency of encounters between aggressors and emitters. However, there are some reports in the literature that indicate that these photocyte-flash emitters do produce brief flashes of light upon contact with motile organisms, usually potential predators. These include dinoflagellates in response to copepod activity (Esaias and Curl, 1972; White, 1979), copepods in response to euphausiids (David and Conover, 1961), hydroids in response to caprellids (Haberfield, 1980), squids in response to shrimps (Young et aI., 1982), ophiuroids in response to several benthic crustaceans (Morin and Basch, unpublished), and pennatulaceans in response to brachyuran crabs (Morin, unpublished). There is even less information about the outcome of these inter- MORIN: COASTAL BIOLUMINESCENCE 805 actions. Copepods have been shown to consume luminescent dinoflagellates at a slower rate than non-luminescent dinoflagellates of the same species (Esaias and Curl, 1972; White, 1979), but the mechanisms involved in the deterrence were unknown. Recently, Buskey et al. (1983) have shown that dinoflagellate lumi- nescence increased the swimming speed, increased the number of swimming bursts and decreased changes of direction in predatory copepods all of which tend to separate the predator from the prey. I also have preliminary evidence that isopods and flatfishes reorient away from an artificial light flash when it is presented near their eyes (Morin, unpublished). Clearly, as indicated for aposematism (Harvey et aI., 1982), more experimental data are needed on the avoidance behavior of the aggressor in response to contact flash signals. Flash Bulb Effect. - Temporary blinding from a luminescent flash is a very pos- sible function for deterring visually orienting and nocturnal foraging predators. Nocturnal predators probably have a visual threshold at less than 10-9 IJ,W cm-2 (Nicol, 1978; Lythgoe, 1979) while most luminescent events are at least two to three orders of magnitude above this level and may be brighter than 10-2 IJ,W cm-2 (Table 2). Since the visual system would be very near the point of contact, it would almost certainly receive the full brunt of the high intensity display. Such a flash would impair the foraging ability of the predator until it has re-dark adapted. Decoy Effect.-In contrast to flashes which deflect an aggressor, glowing lumi- nescence probably serves as an attractant to potential predators (Table 3). For instance, in the dark, large predatory sharks have been shown to more readily attack lutjanid fishes with small implanted lights in their sides than fishes without lights (Moeller et aI., 1972). In darkened tanks, glowing fecal pellets or excised pieces of glowing leiognathid light organs were always ingested by nocturnally active apogonid fishes while comparable non-luminescent materials were not (personal observation). Furthermore, glowing luminescent organs from fishes have long been used by island inhabitants to catch large predatory fish (Harvey, 1952) and, more recently, commercially available chemiluminescent light sticks (Cy- alume Lightstick, American Cyanamid Co.) have been used by fishermen to catch swordfish at night. However, in nearly all cases of coastal luminescence where the duration oflight exceeds about 2 sec either (I) complex behavior permits protection from predators (Morin et aI., 1975; see below), (2) the light acts as an advertisement (see below) or (3) the glowing light is produced as a decoy at a distance from the emitting organism, especially its vital parts (Dahlgren, 1916). There are two common categories of such glowing decoys: sacrificial lures and deluding clouds. In species with sacrificial lures, especially represented by ophiuroids and polynoids, there is a repellent contact flash response upon initial stimulation, but with persistent stimulation the emitting structure (arm or elytrum) is autotomized and the signal switches to an attracting glow (Brehm, 1977; Herrera, 1979). This glowing light is then at a distance from the cryptic, non-luminescing potential prey. The signal changes abruptly from flashes, which repel the aggressor away from the potential prey, to an attracting glow of the jettisoned body part that is well separated from the darkened prey. The glowing ophiuroid arm also writhes around in much the same way that a sacrificed lizard's tail does under analogous conditions of pred- atory attack. Luminescent clouds also tend to be projected away from vital body parts. Numerous observers have often wondered why tubicolous or boring organisms such as chaetopterid worms or bivalve molluscs should produce an internalized luminescent secretion (Harvey, 1952; Dahlgren, 1916). In all these types of cases 806 IJULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983 however, the cloud is projected into the main flow stream of these internally filtering organisms. These same passageways are frequently invaded by a wide variety of commensal animals such as crustaceans, polychaetes and fishes, and provide direct access for numerous small predators such as flatworms, nemerteans, polychaetes, crustaceans and fishes. A large proportion of the motile marine ben- thic invertebrates and many fishes are small and probably capable of crawling or swimming into the tubes and siphons of these sedentary luminescent emitters. Thus it is not particularly surprising that luminescence might be produced deep within their seawater canals. Perhaps the light is intense enough within the confines of these cavities to effectivcly drive out the generally photophobic tube wanderers that patrol these various unique habitats. They are the luminescent equivalents to miniature fire-breathing dragons. Organisms that produce a glowing slime with contact stimulation, e.g., some hemichordates, probably use the light for dual purposes. First, when the light is produced they quickly move away from it, thus producing an attractive glow at a distance from the vulnerable body. Secondly, the light may act as a warning (aposematism) since most hemichordates are known to be distasteful (and apo- sematically colored as well). Species that produce glowing spots of light in the water column, such as ostra- cods (Morin and Bermingham, 1980) and syllid polychaetes (Markert et aI., 1961), appear to use their light for courtship and mating purposes (see below), but in a manner so as to confound potential predators. Since the spots of light are inter- mittently placed and at a distance from the dark emitter, the source is difficult to locate by the predator. Thus these glowing sources can direct a conspecific into the vicinity of the emitter while not disclosing the exact location of the emitter to potential predators and also attracting the predator away from the emitter itself. Burglar Alarm EfJect.-A burglar alarm effect could evolve concomitant with or subsequent to any of the repellent flash or attractant glow signals. In this case the signal functions to attract a predator of the aggressing organism and thereby remove the aggressor by a second order predatory interaction (Burkenroad, 1943; Buck, 1978; Porter and Porter, 1979). There is only limited direct evidence to substantiate the hypothesis. The tendency for motile predators to be attracted to distant light stimuli of varying temporal sequences (see above) is a requisite feature for the evolution of this interaction. I have observed that juvenile, nocturnally foraging kelp bass, Paralabrax clathratus, are more often detected close to the ophiuroid Ophiopsila that have been induced to luminesce by nocturnally active pagurid crabs, than to non··luminescing Ophiopsila (Morin and Harrington, un- published). Furthermore, the evolution of the black screening of visceral masses by many motile marine animals (burglars), especially fishes, crustaceans and ceph- alopods, is presumably a mechanism used by aggressors to conceal ingested lu- minescent prey (McAllister, 1961) and thus reduce attracting the attention of their own predators. This protection is often only partially successful. For instance, on a reef in the Caribbean Sea at night I have observed a fish (Holocenlrus rufus) attack and consume a small apogonid fish (Phaeoptyx conklini) whose oral cavity glowed from the secretion of an ostracod (Vargula bullae) it had captured about 5 sec before (Morin and Bermingham, unpublished). Finally, the results of the flash bulb effect (see above), where an aggressor (burglar) is temporarily visually limited, would also enhance the probability that the predator could approach and successfully remove the aggressor. In a more peripheral way, the contact flash signal is probably used as an indirect burglar alarm (i.e., the mine-field effect of Young, 1983) by a wide variety of large MORIN: COASTAL BIOLUMINESCENCE 807 nocturnal predators who cue in on the light from dinoflagellates that have been stimulated by other organisms but which are not themselves feeding directly on the dinoflagellates (Hobson, 1966; Hobson and Chess, 1976). Species of fish can even be identified at night simply by the pattern of luminescence elicited from dinoflagellates when these fish swim (personal observation). Furthermore, Hobson et ai. (1981) suggest that the tendency for nocturnal marine predators to stalk their prey and then attack swiftly has evolved to reduce risk to themselves because of triggering dinoflagellate luminescence and thereby jeopardizing themselves to still other predators. While more data are needed to verify the existence of the burglar alarm effect, what data there are do indicate that it is an important function that is involved in many types of luminescent emissions. Camouflage Effect.-A final method for evading predation using luminescence is to use the light to prevent a visual aggressor from detecting the potential prey, i.e., concealment by some means of visual deception (Table 3). Most organisms exist in at least a weakly lit environment. An organism in this ambient light will produce a silhouette to any visually orienting predator that is observing from below. Many diurnal marine animals obscure this silhouette by countershading (Denton, 1970; 1971). However, animals active at low light levels appear to obliterate or reduce their shadow with luminescence (Hastings, 1971; Young and Roper, 1977; Warner et aI., 1979; Ngai, 1981). This method appears to be par- ticularly important in the open ocean at depths where light levels are below \0-1 J.LW cm-2 (Young et aI., 1980; Young, 1983). In coastal organisms such counter- illumination capabilities probably occur only among the fishes with gut associated glandular light organs (Ieiognathids, some apogonids and pempherids) or with ventral photophores (batrachoidids and perhaps some sciaenids and engraulids) (for review see Morin, 1981). For maximum protection, the luminescence should exactly match the down- welling ambient light in angular distribution, intensity and color. However, the matching need not be exact in order to provide at least some benefit to the emitting organism. In mid waters where the light is relatively predictable over time with respect to direction, intensity and color, the ability to match seems to be very precise and well developed (Latz and Case, 1982; Young et aI., 1980; Young, 1983). In a midwater organism this concealment is usually produced by the con- certed action of many photophores. In coastal waters the photic environment is much more complex and variable, and depends, among other things, on bottom topography, turbidity and cloud cover. The photic regimen can vary quickly even over short distances and brief periods of time. Thus, using counterillumination 2 in shallow water at low ambient illumination « \0-1 J.LW cm- ) for concealment from predators must be complex and difficult. Continuous and exact matching of the photic background is even more difficult than it is in the open sea. Even so, some degree of matching would still confer some selective advantage over none at all and this seems to be what occurs among shallow fishes that use luminescence for concealment (Hastings, 1971; Ngai, 1981; McFall-Ngai, 1983). For coastal organisms luminescence is only one of many possible defenses, most of which are associated with environmental heterogeneity (Kerfoot et aI., 1980). For in- stance, leiognathid fishes show distinct countershading, both dark mottling above and silvery below, to reduce their visibility during bright daylight hours but this is probably gradually supplanted by luminescence during the crepuscular periods and at night (McFall-Ngai and Morin, in preparation). Furthermore, the pattern of luminescence in Ieiognathid fishes is not uniform and seems comparable to 808 IJULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983 disruptive or matching coloration (sensu Hailman, 1977) rather than exact coun- terillumination (McFall-Ngai and Morin, in preparation). The luminescence prob- ably serves to break up the pattern of the silhouette rather than to totally obliterate it. Given the very murky water « I to ca. 3 m visibility) where these fishes live, such a strategy is undoubtedly more effective than a uniform glow that could suddenly become obvious as a brighter silhouette against a darker sky if a cloud should pass overhead or if the fish were to enter a more turbid water mass. From this point of view, the ventral luminescence of these fishes (and probably the apogonids and pempherids as well) is better termed disruptive illumination rather than counterillumination. Another interesting feature of most shallow water ventral luminescence is that it is usually produced as diffuse light from glandular light organs rather than as a series of discrete points from photophores, which is the common mode in midwaters. The relatively sharper visual acuity of shallow water predators might necessitate a diffuse luminescent pattern in order to disrupt the silhouette, while many discrete lights might serve the same purpose toward the less visually acute but more highly sensitive eyes of predators in midwaters (Morin, 1981). Nothing is known of other possible forms of concealing luminescence in any coastal organisms, but with more behavioral and ecological research other types of matching, disruptive and mimicking patterns will probably be discovered.

Obtain Prey Luminescence, to be useful in predation, must reside within the potential predator. There are four different, but non-exclusive, ways that the signal could operate (Table 3): (1) to attract potential prey to the predator (lure effect), (2) to visually paralyze prey upon contact (stun effect), (3) to detect prey (flashlight effect) or (4) to prevent the prey from detecting the predator (camouflage effect). Lure Effect. - The predatory equivalent of the decoy effect is the lure effect. To be attracted to the predator the prey must have the visual capability to detect and react to the luminescent signal. Such attraction of prey could be (1) either a simple non-specific phototactic response to light or (2) a direct response to a specific mimetic signal that is used for aggression by the predator (Table 3). Many noc- turnally active animals, especially mero- and demersal plankters, show a distinct positive phototaxis to any glowing light. The photic responses of many of these plankters is positive by night but negative by day. Night lights are widely used by fishermen and scientists alike to attract such plankton. Similarly some coastal organisms, such as the flashlight fish Photoblepharon (Morin et aI., 1975), appear to utilize a luminescent glow to attract plankters. This glowing light from Pho- toblepharon can be seen for many meters under water. They feed primarily on small crustaceans, polychaetes and fishes, all of which show a distinct positive phototaxis towards such light. To further augment this effect these fish form large aggregations just above the reef at night (Morin et aI., 1975). Since glowing objects can also attract potential predators, the capacity to evade such a predator must exist concomitantly with the ability to lure and catch prey. Few luminescent coastal organisms utilize lures for attracting prey. The penalties, in the form of increased vulnerability to predators, seem to make luminescent lures especially risky in organisms with restricted defense capabilities. Therefore, in shallow water only the behaviorally complex nocturnal luminescent fishes, such as anomalopids, leiognathids, apogonids and monocentrids, possess phototactic lures (McFall-Ngai and Dunlap, 1983; Haneda, 1980). For instance, Photoblepharon can effectively MORIN: COASTAL BIOLUMINESCENCE 809 avoid predators by converting its slow glow to a dazzling flashing pattern coupled to a rapid protean swimming mode (Morin et aI., 1975). On the other hand, among the behaviorally complex organisms of the midwaters, lures may occur widely (Young, 1983). The use of specific signals for aggressive mimicry may occur among coastal marine organisms for predatory purposes, but there is no definitive evidence. However, in a terrestrial situation, certain female Photuris fireflies mimic the specific luminescent patterns of female Photinus species in order to lure the con- specific Photinus males to them for predatory purposes (Lloyd, 1975). Stun Effect. - The predatory equivalent of the startle effect (see above) is the stun or paralysis effect. Such a temporary stunning function would again utilize the contact flash signal but in this case it would be used to briefly immobilize the visually sensitive prey just long enough for it to be subsequently subdued by additional procuring devices such as appendages or mucus. This function could give passive suspension feeding organisms (e.g., hydroids, sea pens, ophiuroids, medusae, siphonophores) slightly more time to capture small motile visual plank- ters. As evidence for this function, it has been observed that a nocturnally active polychaete (a syllid or nereid, ca. 3-4 cm long) caused, upon contact, a local luminescent flash from the arm of the suspension feeding ophiuroid Ophiopsila californica, and then the worm immediately ceased its vigorous undulatory move- ments and was subsequently caught and eaten by the ophiuroid (L. Basch, personal communication). Presumably, no other predatory measures such as paralyzing chemicals were involved in this initial event. Flashlight Effect. -Only luminescent organisms that have well developed eyes can effectively use a flashlight for detecting various elements in their surroundings, including not only prey but also predators, their conspecifics and the physical environment (Table 2). In coastal waters apparently only some of the luminescent fishes use their light for viewing their surroundings and detecting their prey. All of these presumed illuminating systems in fishes are situated near the eyes as cephalic glandular light organs or photophores. Such a function for cephalic lu- minescence occurs in anomalopids, some monocentrids (at least Cleidopus), some leiognathids (at least Gazza), perhaps some apogonids (e.g., Rhabdamia), and the batrachoidid Porichthys (Haneda, 1980; Herring and Morin, 1978; McFall-Ngai and Dunlap, 1983; Morin et aI., 1975). In most cases there are substantial struc- tural modifications that allow the light to be emitted directionally, parallel to the viewing field. Presumably, this proximity and alignment reduces the parallax between the eye and the light emitting structure so that tapetal and other reflections from the prey are maximally observable. Since these fishes feed primarily on crustaceans and fishes, most of which possess highly reflective tapetums, this eye shine may greatly aid in prey detection. The light might be used at the same time as a lure to attract the prey closer to the predator. Presumably the ocular posi- tioning oflight emitting structures in many of the active midwater species serves similar functions (Young, 1983). Camouflage Effect. -Concealment is a double-edged sword. Not only can it ef- fectively aid in avoiding predators (see above), but also it can allow closer approach to prey. Therefore, all the arguments posed above can equally apply to prey acquisition as well as predator avoidance. For instance, leiognathid fishes with concealed silhouettes probably are able to forage on visually capable benthic prey more easily than if they were not so concealed. 810 BULLETIN OF MARINE SCIENCE. VOL. 33. NO.4. 1983

Advertisement The light emitted by one species could be detected and acted on by a second species for the mutual benefit of both (Table 3). It would be surprising if lumi- nescence did not serve such mutualistic purposes in coastal waters under certain conditions. However, the only well documented case of mutualism involving luminescence is a terrestrial situation between luminous fungi and nocturnal in- sects. The luminescence of some mushrooms serves to attract specific nocturnal insects much as flowers attract diurnal insects or birds. The fungi benefit by having their spores dispersed by the flying insects and the insects benefit by having a place where they can lay their eggs and where their young can develop in the presence of an adequate food supply (the tissue of the fruiting body) (Lloyd, 1974). In the sea, advertisement seems to be operating between luminescent bacteria growing on fecal pellets or dead organisms and visually cueing nocturnal animals (Robison et al., 1977; Nealson and Hastings, 1979). In this case the attractive glowing object would be consumed by a fish, crustacean or cephalopod. The bacteria would benefit by recycling into a high nutrient environment (the gut tract where they are natural symbionts) and in dispersa1. The animal consuming the bacteria would benefit from the consumed particles and the digestive enzymes such as chitinase that the bacteria produce.

Intraspecific Communication In order for luminescence to be used for communicating information between two conspecifics, at least one must emit the light and the other must be able to detect and react to the light. In most known cases both emit and perceive light. Intraspecific communication is primarily the realm of organisms with well de- veloped nervous and visual systems and complicated behavior. These include crustaceans, cephalopods, fishes and a few annelids. There is really no limit to the ways that light could be used, but the simplest and best documented include using the light for reproductive and spacing purposes (Table 3). Studies of intra- specific communication are few and are best known for the fireflies (Lloyd, 1977). In coastal waters luminescence is known to play an important role in sexual reproduction among the polychaete Odontosyllis (Markert et a1., 1961; Wilkens and Wolken, 1981), the ostracod Vargula (Morin and Bermingham, 1980; Ber- mingham and Morin, unpublished), the anomalopid fish Photoblepharon (Morin et a1., 1975; Morin and Harrington, unpublished), and probably the leiognathid fishes (McFall-Ngai and Dunlap, 1983; in review). In Odontosyllis and Vargula the signaling pattern appears somewhat analogous to the intermittent signals of most fireflies and apparently functions similarly in allowing mates to locate one another. The actual role ofluminescence in courtship and the induction of mating is not certain. Individual Odontosyllis and Vargula spend most of their lives in the sediments and crevices of reefs and only venture into the water column above the reefs about an hour after sunset. Significantly, the peak crepuscular predation period of the major reef predators ends about this time (Hobson, 1972; Hobson et a1., 1981). The intermittent displays of Odontosyllis and Vargula, which further make predation difficult (see above), occur repeatedly for only a brief 30-60 min interval whereupon most ofthe individuals return to the reef. In addition, Odon- tosyllis displays only for a few nights near the time of the full moon, while Vargula displays only when the moon is not visible. In anomalopid fishes such as Pho- toblepharon and Anomalops, the sexual luminescent patterns appear to involve more complex interactions. They apparently involve two partners who maintain a strict segregation from their con specifics, often in a separate territory. Blinking MORIN: COASTAL BIOLUMINESCENCE 811 patterns between the two individuals show distinct sexual dimorphism and an intricate interplay between the partners (Morin et aI., 1975; Morin and Harrington, in preparation). These luminescent patterns may represent the most complicated communication system known for visually signaling luminescent organisms. A role for sexual communication using luminescence in leiognathid fishes is inferred from the marked light organ sexual dimorphism that exists in most species of this family (Haneda and Tsuji, 1976; McFall-Ngai and Dunlap, in review). Luminescence probably plays an important spacing role among the fishes in coastal waters. In addition to using luminescent displays for maintaining sexual territories, anomalopids also apparently use their lights to form and maintain large aggregations (Morin et aI., 1975; Morin and Harrington, unpublished; Her- ring and Morin, 1978). Whether or not luminescence is important in this regard in other shallow water luminescent fishes (e.g., leiognathids, pempherids, apo- gonids) that form facultative aggregations is unknown. While more complicated communicatory functions involving luminescent sig- nals may occur in coastal organisms, particularly among the fishes, there are no data available at this time.

Multiple Functions For all coastal luminescent organisms, avoiding or foiling predation would seem to be a prerequisite before additional functions can occur. As we have seen, many shallow water luminescent organisms apparently use their light solely as a mech- anism to deter predators. Where other functions appear to be operating, they also seem to be designed to provide protection from predators. For example, where predatory lures or sexual signals appear they are produced in such a way as to minimize the probability of predatory attack (e.g., ostracods and syllids) or to quickly switch into an anti-predatory mode (e.g., anomalopids and leiognathids). These organisms have a diel component to their behavior so that predators, using ambient light alone, cannot easily locate the emitter. Thus, in many cases, signals do not commence until at least 50 to 60 min after sunset (Morin et aI., 1975; Morin and Bermingham, 1980; Huntsman, 1948). Multiple functions also seem to correlate well with organism complexity (Table 2) and, in coastal waters, it is within the fishes and, to a lesser extent, in the annelids and crustacea that defensive, offensive and intraspecific functions occur together.

COMPARISON OF COASTAL AND OCEANIC LUMINESCENT SYSTEMS There are several significant differences between the majority of coastal and oceanic bioluminescent organisms (Table 4). Simple anti-predatory functions ap- pear to be the dominant function of bioluminescence .in coastal waters, while complex communication (including defense), which results from the more ho- mogeneous environment and more highly developed luminescent systems, be- come relatively more important in oceanic waters. In general, fewer species of coastal organisms (Table I) are luminescent than oceanic organisms. Of the coastal species that are luminescent, they most often have only simple photocytes (e.g., 81% of the luminescent species in Table 1), produce stereotyped flashes, are sessile or sedentary, have poorly developed visual systems and simple behavior (Table 2). Oceanic species, however, tend to have photophores, complex kinetic re- sponses, rapid movement, well developed vision and behavior (Young, 1983). The dominant luminescent organisms in oceanic waters are the fishes, cephalopods and crustaceans, none of which are well represented in coastal waters with lu- minescent members even though their non-luminescent counterparts are quite 812 BUl.LETIN OF MARINE SCIENCE. VOL 33. NO.4. 1983

Table 4. Comparison of the general trends between coastal and oceanic luminescent organisms·

Coastal Oceanic (benthic, demersal, neritic) (mesopelagic) Major representative groups: dinoflagellates, hydrozoans, crustaceans, cephalopods, fish- anthozoans, ctenophores, es (and also hydrozoans, polychaetes, ophiuroids scyphozoans, ctenophores) Pcrcentage of species that are luminescent: 1-2% 60-80% Structure of the luminescent system: simple photocytes and pho- complex photophores or light tosecretory cells; no diop- organs; with dioptric and tric or accessory structures accessory structures Duration of emitted light: flash of 0.04-2 sec or glow of highly variable from 0.1 sec to 5-100 sec; upon contact continuous for minutes to stimulation hours; complex triggering Color of emitted light: variable, mostly green (500- mostly blue (440-500 nm) 540 nm) but some blue (460-500 nm) Visual systems of the lumines- cent emitter: poorly developed or absent well developed and complex Behavioral capacity: limited and simple complex Motility: sessile or sedentary highly motile, swimming Mode of feeding: suspension feeder or auto- active predators, mostly car- trophic nivorous Habitat: enormously complex, very relatively homogeneous heterogeneous in both space and time Ambient light levels: 10' to 10-16 J1W cm-' 10-1 to 10-21 J1W cm-2 Primary functions of the lumi- nescence: to deter predation multiple and variable (includ- ing anti-predation)

• These comparisons are for the overalllrends (see text); overlap and exceptions do frequently occur in both habitats. abundant in the nocturnal fauna. This difference is probably primarily due to the greater complexity of the environment and highly variable light levels in coastal situations which allows alternative biological mechanisms for survival to be uti- lized in place of luminescence. All of these comparisons taken together tend to suggest that luminescence may exhibit significantly different, although potentially overlapping, functions between these two major habitats.

CONCLUSIONS AND PROSPECTS In this paper I have presented a framework that has ecological perspective, so that we can better focus on the questions of the functions of luminescence in all light emitting organisms. Much more behavioral work needs to be accomplished before we can unequivocally define the various categories I have outlined above. Luminescent signaling often does serve multiple overlapping functions for an organism, but even for the simplest kind of anti-predatory signal, we know very little about the details of the interactions. In addition, luminescence is often only one of a suite of anti-predatory defenses utilized by an organism. The sequential and composite interplay between luminescence and other prey defenses, such as diurnal color crypsis or warning, mechanical and chemical weaponry, speed and agility and temporal activities, appears to represent a fertile area for future study. In this same vein, much is becoming known about the role of reflected environ- mental light in animal signaling, especially in terrestrial situations (Baylis, 1979; MORIN: COASTAL BIOLUMINESCENCE 813

Hailman, 1977; 1979). Distinct paralIels can be found between these reflected light signals and luminescent signals. In fact, it would appear that luminescence is an extension and, in some ways, an enhancement of this intricate ambient photic environment. Many of the approaches used in studying reflected light can equalIy apply to bioluminescence. Detailed studies of bioluminescence might prove very powerful in understanding visual communications in general.

ACKNOWLEDGMENTS

I thank P. V. Dunlap, C. Galt, M. Grober, 1. W. Hastings, M. 1. McFall-Ngai, K. Nealson, E. Ruby, S. Strand, R. E. Young and L. Basch, for reviewing the manuscript. However, 1 am responsible for the opinions of this paper and they may not necessarily reflect those of the reviewers.

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DATEACCEPTED: February 16, 1983.

ADDRESS: Department of Biology, University of California, Los Angeles, California 90024.