Chemoreception in Larval Herring and Plaice

Abstract

The fact that fish possess a sense of smell has been known for some time. Fabricus (1780) described how lampreys and sharks would follow rotting meat and Mono, (1744) demonstrated that fish would react to a worm in the water and show adaptation to its odour. Bateson (1890) showed feeding responses in both elasmobranchs and teleosts to hidden food and juices squeezed through cloth. These reactions are present in both seeing and blind fish. Copeland (1912)and Parker (1914) shoved that dogfish were able to localize hidden food by olfaction, thus proving that it could be a directional sense. Initially the study of chemosense had been performed by observing the occurrence of a definite feeding reaction either as a result of detecting food odour or to extend the type of stimulus studied when the reaction had been conditioned to another stimulus (Göz, 1941; Teichmann, 1959). Conditioning is a long process and requires a suitably hardy species. In many cases where a stimulus not connected with feeding is used to condition a feeding reaction we may learn of sensory acuity in absolute terms but nothing of the natural use of the reaction. To examine more subtle reactions to stimuli. especially those not related to feeding, specialized apparatus had to be developed. This allowed workers to look at how a response would be used by the fish in nature. As well as showing reactions to food and prey organisms fish have been shown to use olfaction in social behaviour both with other species and conspecifics of both sexes. Göz (1941) managed to condition a single, blinded, minnow Phoxinus phoxinus to show a feeding reaction to the odour of another fish species Ictalurus nebulosus not the prey of the minnow. This took many weeks using even the easily-trained minnow. Because of the difficulties and limitations many workers have adopted more direct approaches, Wrede (1932) found blinded minnows (a shoaling species) preferred to visit a compartment in an aquarium where the odour of a conspecific lingered rather than a control compartment. Hemmings (1966a) used a more complex preference trough derived from that of Shelford and Allee (1914) and found that the shoaling, freshwater roach (Rutilus rutilus) showed a preference for the end which had the odour of other roach. By analysis of movement in the trough he showed that this preference was due to increased turning rate. Investigating these pheromones in char, D6ving, Nordeng and Oakley (1974) used electrophysiological methods, recording electrical impulses from the olfactory tract, and found the char was able to identify racial differences in this social identifier. Doving,Enger and Nordeng (1973) proposed a component of mucus to be the pheromone. Interest in amino acids as a possible stimulus to feeding in marine organisms began when Steven (1959) found that glutamic acid produced a feeding reaction in two species of tropical marine fish. Case and (iwilliam (1961) found that a range of amino acids would stimulate a blinded crab to feed when applied to the cheiae This reaction was confirmed electrophysiologically on isolated dactyl preparations, responses being obtained from the dactyl receptors to a range of amino acids. Many workers including Hara et al (1973), Hashimoto et al (1968), Haynes et al (1967) and Suzuki and Tucker (1971) have found similar reactions from the olfactory nerves of teleosts. The long, easily accessible olfactory tract in some teleost species makes them ideal subjects for electrophysiological investigation. The technique of monitoring nerve impulses enables a large number of amino acids to be rapidly tested; the thresholds obtained however may not be those which will stimulate a feeding reaction and hardy species are needed. Most work on chemosense in teleosts has been performed on adult and juvenile fish; this is not surprising since rearing beyond the non-feeding yolk sac stage of many important marine species has only been successful in the last decade. The histology and morphology of the development of the olfactory system has also received little study since Holm (1894) described this process in Salmo salar. He showed that in Salmo salar, which took 90 days from fertilization to hatch, there was no nervous connection between epithelium and brain at 60 days post fertilization but one was found at 83 days post fertilization. The olfactory nerve appeared as the groove closed. Attention has been drawn to this lack of knowledge by Hasler (1957), Johnson and Brown (1962) and Branson (1963). In many of the teleosts so far studied the olfactory system is undergoing development not only for the whole of larval life but beyond into juvenile development. Larval development is a valuable time to study this, and indeed any organ system, since it is changing in physical structure, increasing in complexity and possibly changing in acuity and function. The role of a larva can be in many cases to give the early stages of an organism a different ecological niche from the adult, preventing intraspecific predation and competition for food. Therefore its senses may be used for different purposes to the adult, (for example the use of chemosense and touch in the settlement of Balanus nauplii (Crisp, 1974) a system obviously of no use to the adult). In the case of a nektonic shoaling fish such as the herring with a planktonic non-shoaling larva, there would be a possibility of larvae dispersing over a large area prior to onset of shoaling behaviour. There would obviously be some value in keeping larvae together in loose groups and it is likely chemosense may play some part in this. Aggregations of planktonic marine organisms are a well documented phenomena (Barnes and Marshall, 1951; Weibe & Holland, 1968) from the longevity of these aggregations it seems unlikely that this is caused by physical boundaries of water parcels. It seems possible that chemosense acts to keep aggregations intact and in some organisms is retained in adult shoaling life, perhaps to maintain aggregations when the shoals disperse at night (Harden-Jones, 1962). Feeding patterns in larvae and adults can also differ; for example herring and plaice larvae will snap at food organisms in the water column, taking selected individual prey; in the case of herring almost stalking. As adults, herring mainly feed by filtering, although evidence from other filter feeding fish suggest a proportion of particulate feeding will also occur depending on prey size and density (O'Connell, 1972), and plaice move along the sea bed eating epibenthic organisms, mollusc siphons and sedentary worms, Both modes of feeding require good vision. Newly hatched herring (Blaxter and Jones, 1967) and plaice (Blaxter, 1968a) have very different eyes from the adult, the eye developing throughout larval life. In Sardinops caerulea, Schwassmann (1965), the eye is a very rudimentary structure when feeding begins. Although the feeding act is visual, the volume which can be searched using sight alone is small (in herring 0.3- 2.0 litres per hour and in plaice 0.1-1.8 litres per hour (Blaxter and Staines, 1971). It seems possible that olfaction could assist in the search for food either by directionally guiding the fish larva to a concentration of food organisms or restricting energy-requiring searching behaviour to periods when food organisms can be detected by presence of their odour. With these possibilities in mind the outline of study below was adopted.