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Coastal Bioluminescence: Patterns and Functions

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Coastal Bioluminescence: Patterns and Functions 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
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