Induction of trypsinogen secretion in herring larvae (Clupea harengus)

Mechanisms initiating trypsinogen secretion were studied in laboratory reared herring larvae (Clupea harengus L.) exposed to physical and chemical stimuli. Pancreatic secretion of trypsinogen was quantified for each stimulus type as the increase above pre-stimulus level of intestinal trypsin content. Larval prey types were: nauplii, copepodites or adult Acartia tonsa, small polystyrene spheres (diameter 94 m), small (diameter 79 m) or large (diameter 170 m) polystyrene-latex spheres. Intestinal trypsin content can be expressed as a function of two variables: meal size and content of pancreatic trypsinogen. Trypsinogen secretion increases with different prey items in the order: small spheres, nauplii and copepodites. Larvae which eat large spheres secrete more enzyme than if fed small spheres but trypsinogen secretion is similar in fish larvae fed copepodites and large spheres. The fact that the size of non-biodegradable particles exerts a major control over trypsinogen secretion suggests neural — as opposed to chemically mediated — initiation of secretion. A cephalic phase of secretory stimulation could not be demonstrated during swallowing of copepods or exposure for 2 to 3 h to compounds which leak from live copepodites. As cephalic and gastric phases of secretory stimulation are absent, initiation of trypsinogen secretion must take place in the intestine. Larval herring retain trypsin in the intestine. Ca. 4.5 h after a meal, 3/4 of the enzyme is located in the intestinal fluid, presumably available for hydrolysis of subsequent meals, and the high proportion (ca. 25%) of the pancreatic trypsinogen content which is secreted for copepodite prey may thus not be energetically wasteful for the larvae.     

Osmotic properties of eggs of the herring Clupea harengus

Yolk osmolality of developing eggs of the herring Clupea harengus L. is strongly hypoosmotic to seawater: about 440 mOsm during the first week of development decreasing to 360 mOsm before hatching. The perivitelline fluid (PVF) of the eggs is isoosmotic to the ambient medium. The PVF equilibrates within 10 min to changes in the ambient seawater. The content of Na⁺, K⁺, Cl^- and free amino acids amount to 26, 52, 48, and 54 n mol egg^-1, respectively, on Days 1 to 3 after fertilization, increasing to 63, 69, 80, and 79 n mol egg^-1, respectively, prior to hatching (Days 18–20). The apparently conflicting findings of a decreasing yolk osmolality and a simultaneous increase in the amount of egg solutes are at present unexplained.     

Feeding ecology of herring (Clupea harengus) larvae in the turbid Blackwater Estuary

Most studies on feeding by herring larvae (Clupea harengus) have taken place in clear, open waters, but several herring stocks around the world spawn in inshore and estuarine regions. An example is the spring-spawning Blackwater Estuary (Essex, England) stock. Samples were collected in this estuary to examine prey selectivity and feeding levels in relation to biological and environmental conditions. Herring larvae negatively selected copepod nauplii, but positively selected the copepodite and adult stages of Acartia spp. Gastropod larvae were also positively selected. Particles >150 μm width were preferred, whilst particles smaller than this value were preferentially rejected. Concentrations of potential prey items in the water were in the range of 6.0 to 49.7 organisms l⁻¹ with a median concentration of 15.0 organisms l⁻¹ (n = 26). These values are towards the low end of prey concentrations quoted in the literature as being required to sustain herring larval growth and survival. However, theoretical considerations suggest that, in this environment, levels of tidally-induced turbulence enhance encounter rates between larval herring and their prey. On the other hand, turbidity is also related to tidal current speed and might reduce feeding success by decreasing underwater light levels. Measurements at two sites in the estuary confirmed that tidally-induced turbidity reduced the effective water depth in which herring larvae could visually feed by up to 50% at times of peak current speed. However, with the gut-content data available in the present study, it was not possible to discern any clear relationships between feeding success and the state of the tide. Feeding success appeared to be more strongly influenced by surface light-levels. Received: 24 June 1998 / Accepted: 17 February 1999     

High natural mortality of Baltic herring (Clupea harengus) eggs caused by algal exudates?

Results from field studies in 1978 and 1982 together with results from a laboratory study carried out in 1984 indicate that the unusually high natural mortality of Baltic herring (Clupea harengus L.) eggs observed in situ is presumably caused by toxic exudates released by filamentous brown algae during a limited period which happens to coincide with the peak of spawning. Oxygen deficiency is no longer believed to be the major cause of the observed unnaturally high mortality. It cannot, however, be entirely ruled out.     

Variations in sperm motility of the Atlantic herring Clupea harengus

Sperm characteristics and fertilization success were measured in two groups of Manx autumn-spawning herring, Clupea harengus L., captured 1 wk apart. Samples contained motile sperm for up to 45 min after activation (average 7 min). Individual spermatozoa were motile for up to 5 min. The activation of individual spermatozoa is probably phased, although the mechanism for the delay is not clear. This can account for the overall low levels of active sperm at any one time, the periodic fluctuations observed in the proportion of motile sperm, and for successful fertilization rates achieved using samples of apparently immotile sperm. The proportion of motile sperm was not affected by the presence of eggs, but the duration of motility was longer when sperm was activated in the presence of eggs rather than in seawater alone. Individual males differed significantly in the duration of motility in their sperm samples and in the fertilization rates achieved, but not in the proportion of motile sperm in each sample. There were no consistent changes in the characteristics of the spawners or the sperm between the two sample dates. Sperm motility and duration of motility were significantly correlated, but none of the sperm characteristics measured was significantly related to fertilization success. Received: 13 March 1999 / Accepted: 20 May 1999     

Light intensity and the feeding behaviour of herring,Clupea harengus

An infra-red sensitive video-recording technique was used to study the effects of darkness and light intensities from 0.0001 to 270 photopic lx on the feeding behaviour of herring (Clupea harengus L.). When offered natural zooplankton, consisting of a mixture ofCalanus finmarchicus, Euchaeta norvegica, Oithona similis, Balanus sp. nauplii, and crustacean nauplii as prey, the fish fed by biting (snapping) at light intensities above a threshold of 0.001 lx and were size-selective, taking the larger organisms first. When fed on pure cultures of CaliforniaArtemia sp. nauplii (San Francisco Bay brand), the threshold light intensity was 0.01 lx. Swimming speed increased with increasing light intensity when the fish were actively feeding by biting. When the fish were filter-feeding on high densities ofArtemia sp. nauplii in the light, they continued to school and swimming speed was not related to light intensity.     

Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae

Eggs from spring spawning stocks of herring (Clupea harengus L.) were fertilized and reared at either 5, 8 or 12°C in 1991 and 1992. The differentiation of myotomal muscle fibres was investigated in relation to the development of other organs and tissues using light and electron microscopy. The gut, notochord, eyes and haemocoel appeared at the same relative point in development between fertilization and hatching at all temperatures. In contrast, the formation of the spinal cord, pronephros, pectoral fin buds and muscle fibres was relatively retarded at 5°C compared with 8 and 12°C. Myogenesis in the presumptive inner muscle mass occurred after 12 to 16 d at 5°C, 7 to 10 d at 8°C and 3.5 to 6 d at 12°C. Myoblasts aligned in orderly rows running from myosept to myosept prior to fusion to form myotubes. Actin and myosin filaments were synthesised throughout the cytoplasm in associated with presumptive Z-lines at the periphery of myotubes and immature muscle fibres. Differentiation of the superficial and inner muscle fibres types of larvae occurred at around the same time. Following this initial period of myogenesis, the number of myotomal muscle fibres remained constant until after hatching, so that increases in muscle bulk in the late embryo were entirely due to fibre hypertrophy. At hatching, the number of superficial muscle fibres present in myotomes just posterior to the yolk-sac was significantly less at 5°C (108±12) than at either 8°C (132±10) or 12°C (140±10) (mean±SD, 12 fish/temperature). In contrast, there were around 280 inner muscle fibres/myotome, comprising 90% of the trunk cross-sectional area, at all three temperatures. Myofibrillargenesis occurred relatively slowly at low temperatures, so that the volume density of myofibrils in the inner muscle fibres of larvae at hatching was significantly less at 5°C (39.2±9.0) than at either 8°C (49.6±8.8) or 12°C (50.2±9.8) (mean ±SD, 20 fibres/temperature from total of 5 fish). Undifferentiated myoblasts remained at hatching to form a population of presumptive myosatellite cells. The number of presumptive myosatellite cells per mm² cross-sectional area of muscle fibre was more than two times higher at 8°C (1493±335) than at either 5°C (478±102) or 12°C (924±233) (mean±SD, 5 fish/temperature). The results suggest that temperature can influence the commitment of myoblasts to differentiation at a critical stage in embryogenesis, thereby providing a potential mechanism for influencing future growth characteristics. Correspondence to: I.A. Johnston at Gatty Marine Laboratory     

RNA:DNA ratios and growth of herring (Clupea harengus) larvae reared in mesocosms

Autumn-spawned North Sea herring larvae (Clupea harengus L.) were released in two outdoor mesocosms of 2500 m³ (A) and 4000 m³ (B). The mesocosms were monitored for temperature, salinity, oxygen, chlorophyll a, zooplankton and herring larvae abundance. The density of suitable prey for first feeding larvae (mainly copepod nauplii) was initially low in Mesocosm A (<0.11^-1) compared to in Mesocosm B (>11^-1). Half-way through the experiment the situation was reversed, with higher densities of prey in Mesocosm A (>31^-1) as compared to Mesocosm B (～11^-1). The average temperature declined steadily in both mesocosms from 18°C at release to 11–12°C by the end of the experiment 60 d later. The RNA:DNA values of individual herring larvae were related to protein growth rates and temperature adjusted according to Buckley (1984). A corresponding DNA growth index (Gdi) was given as: Gdi=0.68 TEMP+3.05 RNA:DNA-9.92. The RNA:DNA based growth indices were significantly correlated with other somatic growth estimates. The average estimated protein growth rate in the two mesocosms followed the same temporal pattern as the somatic growth rate, but with a lag of 2 d or more. Residual analysis of the regression of ln RNA versus ln DNA also showed the same temporal pattern as the RNA:DNA ratios, but the shift in condition as estimated by this method occurred more in synchrony with the other somatic growth measures. Larvae in Mesocosm A had RNA:DNA values similar to the starvation control kept in the laboratory the first days after release, confirming that larvae in Mesocosm A initially were in poor nutritional condition. On the other hand, the majority of the herring from Mesocosm B were characterised as starving or in poor nutritional condition towards the end of the experiment. The assessment of growth and nutritional condition were in accordance with independent survival estimates which suggested that the majority of the total mortality occurred during the first 15 d in Mesocosm A and there-after in Mesocosm B.     

Variations in the content of trypsin and trysinogen in larval herring (Clupea harengus) digesting copepod nauplii

Trypsin and its proform trypsinogen were quantified by radioimmunoassay in herring (Clupea harengus L.) larvae subjected to different prey densities. During the first weeks of larval life, the enzyme content fluctuated in a threephased pattern. Yolk resorption (Phase 1) was characterized by an increase in enzyme. During the first few days after yolk resorption (Phase 2), there was a sharp decline in enzyme. Older larvae (Phase 3) exhibited a second period of intensive enzyme synthesis. Amounts of trypsin in intestines of feeding larvae were analysed. At first feeding, a basal level of gut enzyme of approximately 30ng was recorded, and the amount of additional enzyme secreted from the pancreatic tissue into the intestine appeared to be dependent upon the numbers of prey items ingested. The enzyme-substrate ratio in the intestine was approximately 1 to 4. Prey availability affected amount of trypsinogen. Larvae experiencing a high prey density had an approximately two-fold higher specific enzyme content in Phase 2 compared to larvae exposed to a low prey density. A proposed nutritional strategy for first feeding herring larvae is discussed.     

Parasites in larvae of the herring (Clupea harengus L.) fed with wild plankton

In winter 1965/66 larvae of Downsherring were reared in aquaria at the Marine Station of the Biologische Anstalt Helgoland. They were fed with wild plankton caught on Helgoland Roads. About 10% of the actively feeding larvae were lost due to two endo-parasites and two ecto-parasites. The endoparasites are: a nematode (Contracoecum sp.) which is taken in by the larvae with the food and enters the host's body cavity from the gut, and a cestode (Scolex pleuronectis) which is found in the posterior part of the gut. The ecto-parasites are: a copepodite stage of a lernaeocerid, which attaches itself preferably close to the anus area of the herring larvae, and the copepode Caligus rapax. The nematode and copepodite were observed when the larvae had reached a total length of 9 to 13 mm. The cestode was found for the first time in larvae of 15 to 18 mm, and Caligus rapax in larvae of 20 to 25 mm total length.     

Escape behaviour of solitary herring (Clupea harengus ) and comparisons with schooling individuals

The escape behaviour of solitary herring (Clupea harengus L.) startled by a sound stimulus was observed by means of high-speed video-filming. The results were compared with data from a previous study on the escape behaviour of schooling herring. Escape responses were divided into “away responses” and “towards responses” according to the orientation of the C-bend of the body relative to the stimulus. The proportion of away responses was smaller for solitary than for schooling herring. In solitary herring, the subsequent escape trajectories of fish making initial away responses showed a bimodal pattern of distribution, with modes at 130 and 180° from the stimulus. Trajectories following towards responses, however, were mainly within the semicircle directed at the stimulus, and their pattern of distribution differed from that of away responses. This result contrasts with observations on schooling herring, whose trajectories following both initial away and towards responses are directed away from the stimulus. In addition, we measured the response latency, defined as the interval of time between stimulus presentation and the first detectable movement of the fish. Solitary herring showed a higher proportion of short-latency responses (latency <50 ms) than schooling herring. Different behaviours appear to be exhibited by herring depending on whether they are solitary or within a school. We hypothesize that schooling may raise the threshold for initiation of fast escape responses, giving longer latencies and slower responses which are more appropriate in their directionality and reduce the possibility of collisions with neighbours. In addition, we suggest that schooling behaviour enhances the directionality and co-ordination of the escape response of the whole school, possibly increasing the probability of surviving a predator attack. Received: 2 October 1996 / Accepted: 17 October 1996     

Effect of temperature on the escape responses of larval herring,Clupea harengus

Herring (Clupea harengus L.) larvae from spring and autumn spawning stocks were reared at different constant temperatures from 5° to 17 °C. At equivalent developmental stages, the spring larvae were longer than the autumn larvae and the larvae reared at low temperatures were longer than those reared at high temperatures. At hatching and at the end of the yolk-sac stage, the larvae were induced, by a probe, to make C-start escape responses, which were recorded and analysed using a high-speed video recording at 400 frames s^-1. The response was rapid and of short duration. The tailbeat frequency and swimming speed were measured during the burst of swimming following the C-start at different test temperatures and in larvae with different temperature histories. The tail-beat frequency was strongly temperature-dependent, rising from 19 Hz at 5 °C to 37 Hz at 17 °C with no effect of temperature history, season or developmental stage. The burst-swimming speed ranged at hatching from 75 to 90 mm s^-1 at 5 °C to 110 to 160 mm s^-1 at 17 °C and at yolk resorption from 90–115 mm s^-1 at 5 °C to 175–190 mm s^-1 at 17 °C. The longer, spring-spawned larvae swam faster than the shorter autumn-spawned larvae. When the swimming speeds were expressed as body lengths (L) s^-1, these differences disappeared. Larvae swam from 7–9 L s^-1 at 5 °C to 15–20 L s^-1 at 17 °C at hatching, and from 8–9 L s^-1 at 5 °C to 15–17 L s^-1 at 17 °C at yolk resorption. There was, however, a significantly faster specific swimming speed by the larvae reared at 12 °C in spring 1991.Honorary Research Fellow of the Scottish Association for Marine ScienceUnfortunately, Karen Fretwell was drowned in an accident on 9 January 1993     

Otolith ring deposition in relation to growth rate in herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae

Larvae of Clyde spring-spawning Clupea harengus L. and hatchery-produced Scophthalmus maximus (L.) were reared from hatching through metamorphosis in 1980 and 1981 in laboratory tanks and in large enclosures under various light, temperature, and feeding regimes in order to study otolith ring deposition and growth under different conditions. Ring deposition and growth rates were significantly affected by rearing conditions in both species. The ring deposition rates observed under the conditions tested ranged from 0.34 to 0.92 rings d^-1 in herring larvae, and from 0.07 to 1.0 rings d^-1 in turbot larvae. Growth rates ranged from 0.11 to 0.42 mm d^-1 in herring and from 0.05 to 0.27 mm d^-1 in turbot. The number of otolith rings was dependent on the growth rate of the individual larva. At the population level, higher ring deposition rates were observed in faster growing populations. In herring larvae, the relationship between average growth rate and average ring deposition rate was logarthmic, reaching an asymptote at 1 ring d^-1 for growth rates approaching 0.40 mm d^-1. The relationship was linear for turbot larvae for the range of growth rates observed.     

Biological effects of oil on early development of the Baltic herring Clupea harengus membras

The effects of petroleum hydrocarbons from two crude oils and one fuel oil (No. 1) were studied on the ontogenic development of the Baltic herring Clupea harengus membras L. Herring eggs exposed to water-soluble fractions of the oils at the time of fertilization showed no decrease in numbers of fertilized eggs compared to eggs exposed 6 or 72 h after fertilization. During embryongenesis, treatment with 3.1 to 8.9 ppm or 3.3 to 11.9 ppm total oil hydrocarbons from light fuel oil and the two crude oils respectively, gave rise to alterations in embryonic activity, decreased heart rate, and premature or delayed hatching. Although many larvae hatched from eggs exposed to contaminated water (3.1 to 11.9 ppm total oil hydrocarbons), the majority of the (70 to 100%) were malformed or dead 1 day after hatching. Exposure of eggs to 5.4–5.8 ppm total oil hydrocarbons resulted in significantly (P<0.001) decreased lengths of the larvae. Increased temperature (from 9° to 14°C) aggravated the effects of the oils. The results are discussed in relation to the potential effects of oil spills and chronic oil pollution on fish eggs and larvae in the Baltic Sea.     

Factors influencing predation of Hyperoche medusarum (Hyperiida: Amphipoda) on larvae of the Pacific herring Clupea harengus pallasi

Predation of different-sized Hyperoche medusarum (Hyperiida: Amphipoda) on larvae of the Pacific herring Clupea harengus pallasi was studied in the laboratory. The attacking rate of H. medusarum was a function of herring larvae size as well as size of the predator, and varied from 0.15 to 0.95 larvae attacked h^-1 per hyperiid. In the range of 7.55 to 16.05 mm total larval length, vulnerability to predation was highest for 13.3 and 13.7 mm larvae. Large hyperiids swam faster and covered a wider area during searching and were more effective predators than small ones. Predation seemed to be influenced by light, and its intensity was dependent on the duration of previous food deprivation of the hyperiid.This study was sponsored by the International Bureau of the Gesellschaft für Kernenergiever-wertung in Schiffbau und Schiffahrt in connection with the German Canadian agreement on scientific and technical cooperation.     

A laboratory study of predation by Aurelia aurita on larval herring (Clupea harengus): Experimental observations compared with model predictions

Predation by the medusa Aurelia aurita L. on early first-feeding stage larvae of the herring clupea harengus L. was studied in the laboratory. The medusae were captured in Loch Etive, Scotland. Herring larvae were reared from the extificially fertilized eggs of spawning Clyde herring caught in March, 1982. Swimming speeds, volume searched”, capture efficiency and predation rates increased as medusa size increased. Predation rates on fish larvae increased with prey density, but appeared to approach a maximum at high prey densities; in 1 h experiments, a maximum rate of predation of 6.64 larvae h^-1 was estimated by fitting an Ivlev function. A model to predict predation rates was constructed from swimming speeds, sizes and densities of medusae and larvae, and capture efficiency. The rates of predation predicted from the model fell within the range of experimental data, but tended to underestimate rates and did not account for saturation of medusae. Swimming patterns of medusae changed after prey capture: (a) before capture, encounter rates were low and medusae were relatively less active; (b) after capture of 1 larva, encounter rates doubled, with the stimulated medusae exhibiting increased activity and an aftered “searching” path; and (c) after capture of many larvae, swimming speeds and encounter rates of medusae decreased.     

Lipid class and fatty acid composition of brain lipids from Atlantic herring (Clupea harengus) at different stages of development

Little is known about the changes in composition of brain lipids and fatty acids at different stages of development in fish. Wild Atlantic herring (Clupea harengus L.) were collected from Loch Linnhe and the Firth of Clyde, Scotland, from August 1990 to March 1991. Lipid class and fatty acid compositions of brain lipids were studied at four different stages of development: larvae at the end of the yolk sac stage, two juvenile stages and sexually mature adults. The total lipid content in brains increased during development, and larval brains contained higher proportions of neutral lipids and lower proportions of polar lipids than the brains of juvenile or adult herring. Increased proportions of polar lipids in juvenile and adult herring brains were mainly due to increased percentages of phosphatidylcholine (PC), phosphatidylethanolamine (PE), cerebrosides and sulphatides. The increase in the proportions of the glycolipid classes suggested increasing levels of myelination with development. In total lipids, saturated fatty acids generally decreased and monounsaturated fatty acids and dimethyl acetals (derived from PE-plasmalogen) increased from larvae to adults. However, the proportions of polyunsaturated fatty acids in individual phosphoglycerides were generally highest in juvenile stages, due mainly to increased 22:6n-3, and were lowest in adult fish. Relatively high percentages of 24:1 isomers were found in all the phosphoglycerides, but primarily PC, and these increased during development from larvae to adult. Fatty acids were distributed between individual phosphoglycerides with a characteristic pattern that did not change with development, although the relative amounts of individual fatty acids were altered. The variations and roles of the different lipid components of herring brain are discussed with respect to lipid compositions and functions in brains of other fishes and vertebrates.     

Growth and mortality in young larval herring (Clupea harengus); effects of repetitive changes in food availability

Following yolk resorption, laboratory-reared larval Baltic herring (Clupea harengus L.) were exposed to two sequences of food restriction for 5 d and re-alimentation for 10 d. Comparisons regarding larval growth (standard length and content of water-soluble protein), mortality and content of the sum of trypsin and trypsinogen were made with larvae at a continuous high ration. Larvae exposed to varying prey abundance grew less in length than the control, and during the second high-ration period (Day 22 to 32) growth in length ceased. From the first low-ration period onwards, the content of water-soluble protein in these larvae was lower than that of the control larvae, and the survival rate of the low-high ration group was 59% compared to 77% in the larvae at a continuous high ration. In contrast, the effects of varying food availability were minor on larval content of trypsin and trypsinogen. Results are compared with previous findings in larval Clyde herring, and the effects of larval stock and timing and duration of food restriction on larval growth performance are discussed.     

In-situ observations of Baltic herring (Clupea harengus membras) spawning behaviour in the Askö-Landsort area,northern Baltic proper

In a Baltic herring (Clupea harengus membras L.) spawning ground study, carried out in summer 1982 in the northern Baltic proper, spawning herring were encountered on two line transects on June 14. The spawning behaviour of minor groups as well as of a large school was studied in situ by four divers for approximately three hours. No behavioural differences or systematic coordinated behaviour between the sexes could be detected. Most of the spawning took place in a limited depth interval, 0.5 to 4 m, and Ceramium tenuicorne was the substrate most used.     

Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras)

The anti-predator behaviour of Baltic crustacean planktivores was studied in feeding experiments under predation pressure of herring. The experiments were conducted with pelagic mysids: Mysis mixta and Mysis relicta, and with Cercopagis pengoi, a non-indigenous cladoceran, which invaded the Baltic Sea in 1992. Zooplankton was offered as prey. Two kinds of experiments were performed in the absence and presence of chemical predator cues: (1) two-prey experiments with prey, which have poor or good escape responses and all three planktivores and (2) natural prey experiments with mysids in natural zooplankton assemblages. The results showed that all three species reacted to the chemical cue of herring by decreasing their feeding rate and altering prey selection. C. pengoi selected easily captured prey (rotifers) in two-prey experiments under predation risk while selection for any prey was evident in mysids in natural prey experiments only in the absence of predator cues. This indicates that planktivores have different anti-predator strategies, which are modified by their own prey capture abilities. C. pengoi was a very efficient predator on small prey with size-specific prey consumption rate 5 to 18 times the rate of mysids. Results show that the studied planktivores are capable of adjusting their feeding behaviour to decrease their conspicuousness in order to increase survival under predation risk. Further, results support the view that C. pengoi has adapted well to the Baltic ecosystem, sharing food niche with pelagic mysids and most probably having a strong influence on the whole pelagic food web.