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Author: |
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Theodore Holmes Bullock
Department of Neurosciences and Neurobiology Unit
Scripps Institution of Oceanography
University of California, San Diego
9500 Gilman Drive DEPT 201
La Jolla, CA 92093-0201
Phone: (619) 534-3636
Fax: (619) 534-3919
e-mail: tbullock@ucsd.edu
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Introduction |
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Whereas the neural analysis of behavior of planktonic species and stages has been relatively neglected, we have many clues that it is going to be rich, diverse and interesting. The aims of this contribution are to defend that statement, with selected examples, and to suggest that neural analysis, particularly sensory physiology, has great explanatory power of ecologically significant behavior.
I have to begin with a personal note about plankton, recalling the lasting impression made long ago by a film on invertebrates in the Arctic where scyphomedusan jellyfish were pulsing at a rate well within the range familiar in summer temperate waters, warmer by 20º C. I must have been influenced by this observation and my own experiences in a study of the neural basis of fluctuations in the rate of pulsation of medusae (Bullock 1943), some of which was made in December 1941 in Pensacola, where my wife and I collected Rhopilema cruising at random in the Sound, stopped now and then by Army bridge guards concerned about saboteurs in that first fortnight after Pearl Harbor. At any rate, by the early fifties about half of my laboratory group was devoted to the physiological ecology of temperature acclimation in marine invertebrates. That field, which I left in the early sixties, still offers a challenge in the ecologically fundamental question of why some species are able to acclimate much more than others. The proposal I made in 1955, that different rates in the same organism acclimate to different degrees, resulting in greater disharmony in some species than others, may still be viable and most likely applies to rate processes in sensory and central nervous functions, among others.
Medusae are large animals, relatively, although generally treated as planktonic. The first reaction from most workers when neurophysiology of plankton is mentioned concerns their small size or gelatinous nature. The first message I bring is not new but also not widely appreciated.
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Small size and slipperiness are no excuse |
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Technics have been successfully developed to record nerve impulses from single neurons in zebra fish larvae (Eaton and Kimmel 1980). (Only one or a few sample citations are given, here and in the following, often representing a substantial literature). Many papers deal with electrical recording from small flies (Ogmen and Garnier 1994), even Drosophila (Wyman et al. 1984; Elkins and Ganetsky 1990; Engel and Wu 1992; Trimarchi and Schneiderman 1993) and mosquitoes, and from copepods (Yen et al. 1992). Single unit action potentials have been recorded from scyphomedusans (Horridge 1953), Clione (Arshavsky et al. 1988, 1991, 1992; Huang and Satterlie 1990; Satterlie 1993; Norekian 1989, 1993; Norekian and Satterlie 1993b), Melibe (Trimarchi and Watson 1992), a number of other opisthobranchs, and cephalopods (Maturana and Sperling 1963; Laverack 1980; Boyle et al. 1983; Bullock and Budelmann 1991) and larval fish (Eaton and Nissanov 1985 mentions a predatory protozoan causing escape responses in larval zebrafish; Eaton and DiDomenico 1986). Many studies have been done upon unanesthetized animals, free to move and behave, within limits.
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Behavior turns up new senses and forms of recognition to be accounted for |
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The chief source of clues to sensory biology and interesting neuroethology of zooplankters is the close observation of their behavior and responses. I will cite some examples that present opportunities for new analysis of their neural bases.
Responses to pure hydrostatic pressure stimuli have been reported in a number of species (Morgan 1984; Forward, this volume). Following earlier suggestions from much greater stimulus intensities, Knight-Jones and Qasim (1955) Baylor and Smith (1957) and Enright (1961, 1962, 1963, 1967) found responses to changes in pressure as low as 10 cm of water or 10 millibars (mb). Knight-Jones and Qasim provided no details about their experimental methods but reported up-swimming to increases and down-swimming to decreases of 10 mb in Carcinides and Galathea megalops larvae. Baylor and Smith found lower thresholds in pteropods and copepods (Pontella, Temora) and, like the previous authors, thresholds of < 1 atmosphere in annelids, hydromedusae, chaetognaths, ctenophores, copepods and others. According to my memory of their verbal presentation, though not in the brief printed version, Baylor and Smith, in one type of experiment, watched individual zooplankters in a vertical glass cylinder, swimming up and down within a range of a few centimeters. They then raised or lowered a leveling bulb connected to the cylinder - whose top was closed - by a flexible U-tube, following each vertical movement of the animal. Keeping the pressure constant at the level of the animal, it increased its vertical excursion markedly, as though lacking the normal change-of-pressure feedback. This behavior implies a non-drifting, absolute pressure sense. Baylor and Smith report that a 15 cm stimulus causes a 15 cm response in the compensatory direction. They emphasized that reliable responses require animals brought in with extreme care to avoid pressure or pH or other shocks. Depth compensating responses by planktonic animals had been reported in some species to persist with undiminished intensity for several hours (Hardy and Bainbridge 1951, who used stimuli in the 500 mb range), and have therefore been interpreted as indicating a sort of "barostat" by which the animals might maintain constant depth, to within a few meters in the sea.
In contrast to the sustained type of response, which requires a tonic receptor, Enright observed transient but intense behavioral responses in Synchelidium sp., an intertidal, predominantly benthic amphipod. He did not exclude their having some sustained sense but showed the importance of the phasic component. He started with many amphipods in a closed jar of sea water, most of them resting on the bottom. Raising the leveling bulb or adding small weights to a piston, both of which were done in the next room, in double blind experiments, caused many animals to swim about vigorously for a few seconds. Decreasing the pressure caused transient reduction of ongoing spontaneous activity. He later found similar responses in the anomuran Emerita, particularly the megalops larval stages, immediately after they have settled following a prolonged planktonic development. He excluded the possibility of small gas bubbles, and we have no precedent for other structures with appreciable compressibility different from aqueous tissues or with piezoelectric properties immersed in aqueous tissues. Digby (1961) proposed a mechanism involving a monolayer of gas but his evidence has not been generally accepted. Even in the best studied species, Emerita, we do not know where the reception occurs. Enright has observed responses in some individuals after removal of all periopods or all four antennae or both eyes (pers. comm.). I believe a hitherto unknown sense organ, indeed a new class of sense organs is awaiting discovery. Only after localizing and identifying the organ can we expect to deduce the detection principle it employs.
Mechanoreceptors for water movement and vibration are probably among the most amenable to new physiological study (Newbury 1972 in chaetognaths; Wiese and Marschall 1990 in euphausids). Lateral line-like sense organs have been reported in penaeid shrimps (Denton and Gray 1985) and in cuttlefish (Budelmann this volume; Budelmann and Bleckmann 1988; Budelman 1989; Budelmann et al. 1991; Bleckmann et al. 1991a; Bleckmann 1994).
Also awaiting discovery in zooplankton are temperature receptors, especially those with a non-adapting, thermometer-like response that can explain the known behavioral response manifested by a consistent thermopreferendum. It has been repeatedly pointed out that at least teleosts and probably many taxa and stages of development show an ability to stay in a layer of water of a preferred temperature, to within a fraction of a degree, i.e. close to an isotherm. It seems unlikely that this is explainable in the general case by a parallel isodensity (Forward 1989b and this volume) or other clue. If it is, then yet another non-adapting sensory receptor is to be sought. Thermometer organs are well known in mammals, including those that are excited by increases in temperature in the normal living range ("warm receptors") and those that are excited by decreases in temperature in this range ("cold receptors"). They are believed to occur in fish and other exothermic taxa but a convincing demonstration of specific temperature sense organs is an outstanding opportunity (Späth 1978), particularly in zooplanters. The adapting aspect of sense organ response, i.e. a temperature rate-of-change sensibility is likely to be found first, either in separate receptors or as an initial part of the response of thermometer-like receptors (Forward 1990b and this volume). But, the experience with the ampullae of Lorenzini of elasmobranchs warns us to be cautious; they were first thought to be very sensitive temperature change receptors (Sand 1938) and only later this modality was shown not to be the normal adequate stimulus (Bullock 1974).
Chemoreceptors are indicated by many behavioral observations which, moreover, point to high specificity and sensitivity Lazzaretto et al. 1990; Demott and Watson 1991; Kassimon and Hufnagel 1992; Snell and Morris 1993; Bollens et al. 1994, to cite only some of the more recent reports).
Some kinds of behavior have yet to be found, but I believe, will be found in zooplankters and will then trigger the search for the organs mediating it. An example is magnetic orientation, known in bacteria (Kalmijn 1978; Blakemore et al. 1980), where the behavior is apparently adequately accounted for by a known organelle. The behavior has often been claimed for birds and insects but no sense organ or identified transducer has been convincingly shown as yet. Lohmann et al. (1991) report a particular pair of cells in the gastropod, Tritonia, that alter their firing in response to changes in earth-strength magnetic fields; the same field changes do not influence any of 50 other cells.
Magnetic orientation as an indirect consequence of highly sensitive electrosensory organs and central pathways and processors able to extract this information and use it in normal behavior, has been shown in elasmobranchs (Kalmijn 1988). A similar sense exists in some quite small teleosts, marine (Plotosus, Arius, Siluriformes), as well as freshwater (Siluriformes, Gymnotiformes, Mormyriformes and one subfamily of Osteoglossiformes). At present, however, none but the elasmobranchs are known to have an adequately high sensitivity to make use of the currents induced by motion in the earth's magnetic field. Still, neither the sensitivity in these groups, already known to be electrosensitive, nor the existence of this sense in other taxa, both vertebrate and invertebrate, can be categorically ruled out. I anticipate new findings of both electrosense and direct magnetic sense.
Other forms of behavior are quite familiar and yet the sensory modalities involved are only partly or little known. Schooling in teleosts and other groups, including members of the zooplankton, seems likely to depend on more than one sense in different species and conditions (Partridge and Pitcher 1980). I doubt that our present understanding, based on a few species, is a representative picture of this widespread class of behaviors. To mention one example, Kalmijn (personal communication) has suggested that the dense schools of the marine catfish, Plotosus, may under some conditions use their electrosense to keep together.
Other familiar behaviors whose sensory bases are rarely or little known are predator avoidance, prey detection, conspecific communication and mate recognition. Data on fish kairomones that influence the avoidance or swarming behavior of Daphnia are presented elsewhere in this volume (Larsson; Ringelberg and van Gool; DeMeester). Finicky settlement of barnacle, polychaete and other larvae upon substrates according to its "taste" or texture is well known (Johnson and Strathmann 1989; Harvey 1993; Dineen and Hines 1994; Forward, Zimmer-Faust this volume). Long ago I reviewed the literature on predator recognition by invertebrates and found few examples at that time, apart from scallops and freshwater snails (Planorbis); I reported observations of limpets and abalones fleeing from a starfish tubefoot (Bullock 1953b). Specific chemical signals must be much more common than we then appreciated. The swimming escape response triggered by a brief contact with starfish tubefeet in the sea anemone, Stomphia (Wilson 1959) and the nudibranch, Tritonia, (Willows and Hoyle 1969) have been studied physiologically; in the latter case a network of neurons was identified that makes the decision whether to trigger the prolonged behavior.
Complex visual form recognition is indicated by behavior such as the use of dozens of distinct color patterns for as many social signals, shown by Moynihan and Rodaniche (1982) in a Carribean squid (Sepioteuthis). Startle responses are a fertile field, convenient for sensory analysis because they are relatively stereotyped and hence successive experiments are likely to represent the same behavior. In the wide variety of taxa where they are found, different adequate stimuli are known, from a moving shadow to a tap or an acoustic click (Eaton 1984). Mackie (1990) has pointed out interesting parallels between the giant fiber jet swimming in squid and jellyfish, a form of behavior that is not sterotyped but quite flexible (Otis and Gilly 1990). Careful experimental ethology may reveal that in some cases several stimuli of different modalities may function in sequence to bring an animal into close proximity with a desirable target or prime it to be more sensitive to some forthcoming event.
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A point of view makes you a neuroethologist |
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Ecologically significant behavior opens another dimension when we begin to uncover the mechanisms in sensory physiology, central analysis of sensory input, recognition of species characteristic sign stimuli, plastic modulation by age, state or other sensory inputs, selection of response from the species repertoire and neural control of effectors. With emphasis on the sensory side, I will illustrate with a selection of examples from near-planktonic or related or paradigmatic species that have received some successful study. These are intended to underline the opportunities and needs in further extension to the great range of planktonic taxa. It is important to note that, whereas some started with known behavior to be accounted for, others began as bottom-up or inside-to-outside or anatomy-to-physiology curiosity. Sometimes the relevant behavior has yet to be defined.
A good example is the discovery of a sensory system in cephalopods - actually in young, planktonic cuttlefish (Sepia), that appears to be an analogue of the lateral line system in aquatic vertebrates (Budelmann and Bleckmann 1988; Budelman 1989; Budelmann et al. 1991; Bleckmann et al. 1991a; Bleckmann 1994). Anatomical suggestions of possibly sensory structures are widespread (Hayashi and Yamane 1994; Jensen et al. 1994) and led the physiologists in this case to look for responses in the rows of cutaneous organs on the head. They proved to be responsive to disturbances in the water and not to other stimuli - a new modality for molluscs.
Quite a different story is represented by a recent finding in a classical sense organ in a squid (Alloteuthis), the statocyst. Here Williamson (1989) surprises us with the demonstration of electrical coupling between secondary hair (sense) cells - a step toward uncovering the cellular mechanisms of reception. Arkett and Mackie (1988) have shown the sensory hair cells for mechanoreception in the planktonic medusan, Aglantha, to be amenable to physiological study. The same must be true for water movement sensors in many other groups (Budelmann 1989; Bleckmann 1994). The sharp distinction found in vertebrates between the lateral line and the inner ear reception of disturbance in the aquatic medium outside the animal has yet to be properly compared with an adequate sampling of invertebrate systems. A large literature exists on the physiology and anatomy of hearing in fish (Atema et al. 1988; Kalmijn 1988; Popper, this volume), including some small enough to be marginally planktonic and including very young sharks (Bullock and Corwin 1979). A smaller but substantial literature exists on the lateral line (Coombs et al. 1989). One feature of the octavolateral sense organs of vertebrates which may have deep significance for their function in planktonic stages of fish is that the number of sensory hair cells increases with size dramatically. Presumably this confers greater ability to detect feeble signals and one has to wonder whether larvae and young fish are relatively deaf. Whereas well controlled behavioral experiments on adequately motivated animals are the final arbiter, simple electrophysiological endpoints may often be the first way to study such questions as the upper frequency limit of hearing or the influence upon hearing of the developing swim bladder and, in some species, its later disappearance. We found in young yellow-tail tuna (Thunnus albacares) that brain responses to inner ear reception cut off sharply above the remarkably low frequency of 350 Hz, even lower than an earlier report based on conditioned responses in two specimens (Iversen 1967; Bullock, Brill and McClune, unpublished experiments).
Electroreception has already been alluded to. Many species of agnathans, holocephalans, teleosts and others have been shown to be electroreceptive - more readily by physiological than by behavioral responses (Bullock et al. 1961; Bullock and Heiligenberg 1986; Fields et al. 1993). Other taxa with this sense modality seem likely to be found, especially among teleosts, but small size confers a serious disadvantage. Sometimes the technic for recording from single receptors is exceedingly simple and requires no surgery (Viancour 1979; DeWeile 1983).
Photoreception and vision have attracted much attention among invertebrates (Therman 1940; MacNichol and Love 1960a, b; Wiersma et al. 1961; Waterman and Wiersma 1963; Gwilliam 1963; Hartline and Lange 1974; Lange and Hartline 1974; Lange et al. 1974; York and Wiersma 1975; Schiff 1987, 1989; Cronin et al. 1994) including a few studies on planktonic forms (Smith and Macagno 1990; Frank and Widder, this volume). I expect many adaptive specializations to be found among zooplankters - for detecting color, moving shadows, dim light and the like. One which could be overlooked we found in the young tuna midbrain; optic lobe responses show a high flicker fusion frequency, approaching some of the fast eyes in certain insects and nearly double that in humans - presumably an adaptation to aid vision during rapid swimming (Bullock, Brill and McClune, unpublished).
What is taste and what is olfaction? Why are they so distinct in the peripheral and central structures that mediate them in the vertebrates - already in aquatic taxa, long before terrestrial forms evolved? These questions come primarily from the anatomy and physiology but depend on ethology and ecology for essential clues. Taxa differ greatly in the mechanisms of chemoreception and comparative physiology is essential, in parallel with comparative behavior, to understand the dynamic range, degree of specificity, temporal and spatial resolution of these senses.
I like to tell how important taste was in the history of the Scripps Institution of Oceanography and of the unique concentration of neuroscientists in La Jolla. Yngve Zotterman, Professor of Physiology at the Royal Veterinary College in Stockholm, was a prominent comparative physiologist of gustation. He started the series of international congresses on Olfaction and Taste, of which the volume edited by Kurihari, Suzuki and Ogawa (1994) is the eleventh. He visited his fellow Scandinavian, Per Scholander, in La Jolla, in 1959. Scholander was a comparative physiologist of respiration, cardiovascular, water and salt functions and got Zotterman to support his idea of a laboratory vessel dedicated to comparative physiology and biochemistry by showing how he would set up to record nerve impulses from taste fibers in teleosts on board one of the smaller Scripps vessels at sea. Yngve didn't succeed on that trip but supported Pete's idea, which led shortly to the R/V Alpha Helix. After that, one thing led to another until Pete and others at S.I.O. recruited the first neuroscientist to La Jolla, in 1965 - Susumu Hagiwara, who was followed by a swelling stream of like ilk, now many hundreds strong, more than a score of them doing marine biology. In spite of a substantial literature (represented in our reference list by Finger and Silver 1987, Atema 1994, Atema and Voigt 1995), the spectrum of taste receptors and even more of olfactory receptors is still only fragmentarily known, even in the most studied arthropods, molluscs and fish.
In order to do justice to the ecologically significant neuroethology of zooplankters, we have to look a bit farther along the central nervous pathways from sense organ to behavior. I will mention only a few examples from taxa that include planktonic members deserving study.
Giant fiber systems have been evolved again and again, convergently, among the phyla and classes; even orders and families may differ profoundly in the development of these systems (Bullock 1948a, 1953a), usually associated with startle responses and the first phase of escape (Eaton 1984). They are quite amenable to study in small forms, as already pointed out for Drosophila (Wyman et al. 1984), even with extracorporeal, non-invasive electrodes (Featherstone and Drewes 1991). The meaning of the giant fiber diameter cannot always be its greater velocity, for in small animals like Drosophila the absolute saving in time is small. Nevertheless, in some shrimp, adaptations of the giant fiber for high velocity result in phenomenally fast axons - by far the fastest known (Fan et al. 1961; Huang and Yeh 1963; Hsu et al. 1964, 1975a, b; Hao and Hsu 1965; Kusano 1965, 1966, 1971; Hsu 1982; Terakawa and Hsu 1991). This is an elegant case where a simple property revealing a remarkable specialization was overlooked for decades, even though shrimp giant fibers had been studied and shown to be unusual (Holmes et al. 1941).
Motor output, its patterning, and central and peripheral organization intimately complement the sensory input and are sure to be of interest in zooplankters. Some illustrative studies include that of Spencer (1988) showing non-spiking interneurons in the swimming system of a pteropod and of Arshavsky et al. (1988) who found nonsynaptic interaction - both discoveries being of general neurobiological import. Arshavsky et al. (1991, 1992) and Satterlie (1993) represent a series of studies of the organization of the swimming system in these gastropods. Wilson (1960) studied the nervous control of movement in annelids, and Bowerman and Larimer (1976) that in crustaceans. A number of chapters in Sandeman and Atwood (1982) and Wiese et al. (1990) have relevant recent examples. Moss and Tamm (1993) show that even the delicate movements of ctenophores can be successfully studied with electrophysiological methods. Important effectors other than moving major parts of the body include the chromatophores. Some studies on them and their control underline the opportunities (Cooper et al. 1990; Hanlon et al. 1990; Novicki et al. 1990), especially when cephalopods in good condition can be as readily available as they are now (Hanlon et al. 1978, 1983). Nervous control of luminescence is also interesting and approachable (Nicol 1960; Baxter and Pickens 1964; Latz et al. 1990; Bowlby and Case 1991; Bannister 1993).
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Anatomy has many new tools and rich rewards |
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Although our symposium emphasizes sensory ecology and physiology, I must call attention to the opportunities for advancing both of them through anatomical investigation. The armamentarium of available new methods, especially those applicable to revealing neural organization has expanded dramatically in recent years and most of the newer procedures have yet to be exploited on zooplankters. Immunocytochemistry, intracellular dyes and markers transported throughout a neuron and its processes, even in fixed material, laser confocal microscopy and the use of optical signals of activity, with or without voltage-sensitive dyes are some of the technics now in use for identifying and tracing nerve cells and their connections, distinguishing among types of neurons and visualizing active neurons. A limited selection of examples concern the retina (Saidel 1980; Saidel et al. 1983; Cronin et al. 1994; Arikawa and Matsushita 1994; Becerra et al. 1994; Evans et al. 1993; Munz and McFarland 1977). A selection on other sensory and central structures is represented by the reports of Tamm and Tamm 1990; Bollner et al. 1991; Bundy and Paffenhofer 1993). Many sense organs have been long known anatomically, or more recently recognized, but are still without any secure assignment of function. An example is the dorsal organ of many crustaceans, including planktonic taxa (Laverack and Sinclair 1994).
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The coda integrates the themes and leitmotifs |
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Our organizers have rightly called attention to the great gap in understanding the principal fauna of the bulk of the biosphere. However complete our list of species, our zoogeography, foodwebs, and life histories, we cannot claim understanding before we know a good deal concerning what each zooplankter does about food, enemies, mates and other conspecifics, diurnal and seasonal states, what it can recognize and discriminate, what behavior follows each adequate stimulus, the pattern of succession of the behavioral repertoire - and the sensory and neural apparatus that accomplishes vital tasks.
A major development in zoological neurology in the last quarter century has been the discovery that many taxa of invertebrates have a large proportion of their nerve cells unique and identifiable in every specimen, making it possible, bit by bit, to piece together all or nearly all of the circuitry. This should apply at least as much to the zooplankters as to the bulky lobsters and sea slugs. Such encouragement, combined with the message documented above, that small size and slipperiness need not prevent microelectrode recording with controlled stimulation, makes it clear that the time is ripe and the technics available to make real inroads into this massive agenda. The clues and precedents from work already accomplished by pioneers in the area also make it clear that we can expect surprises and major discoveries, not simply smaller versions of familiar neuroethology. Zooplankton, in its marvellous variety, faces a set of problems in everyday living different from those of benthic, littoral and other faunas and not at all uniform or uneventful as we might imagine from our human perspective on their watery world. I look forward to the next convening of this range of specialists since it seems certain that in the interim this meeting will have sparked an abundance of new efforts and fascinating stories.
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References |
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The following list includes titles cited in the text and, at the request of the Editors, others relevant to the subject, selected mainly from recent literature. For the sake of length, many important older references are not included.
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Introduction
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