Irreversible Starvation Research Articles

Observational learning and irreversible starvation in first-feeding zebrafish larvae: is it okay to copy from your friends?

Starvation is one cause of high mortality during the early life stages of many fish species.If larvae do not learn to feed, or if no food is available during early stages, irreversible starvation occurs and larvae reach the Point of No Return (PNR), the developmental period/age when they will not feed even if food is available. Fish larvae may learn to how to feed by observing conspecifics or through personal/individual experience with prey items that are encountered. We examined food acquisition in first-feeding zebrafish larvae to determine the impact of delayed feeding and identify the time of irreversible starvation and the PNR. Next, we examined how feeding ability, and the PNR, is altered by either observational learning or previous experience, to determine which paradigm facilitates successful feeding.Our data indicate that zebrafish larvae learn to feed, with the PNR at 7-8 days postfertilization (dpf). Exposure to prey items immediately after hatching (3-5 dpf) results in the highest survival rates. Zebrafish larvae learning to feed by observing conspecifics also had high survival, though the PNR was not changed. In contrast, previous experience with prey items caused an earlier PNR and reduced survival. Overall, these results that indicate feeding is a learned behavior in zebrafish larvae and interacting with/observing conspecifics during the early larval period is a better predictor of feeding ability than previous experience with food.

Irreversible starvation using RNA/DNA on lab-grown larval anchovy, Engraulis encrasicolus, and evaluating starvation in the field-caught larval cohort

The recruitment of anchovy Engraulis encrasicolus, the crucial forage fish in the Black Sea ecosystem, has drastically decreased in the last two decades, mainly due to overfishing. The wild-caught fertilized anchovy eggs were hatched and the larvae exposed to the different feeding levels to indicate the irreversible starvation criteria based on RNA/DNA, then the nutritional status of wild-caught larvae were evaluated. The newly hatched larvae had mean notochord length of 3.25 ± 0.04 mm and first feeding started on day 3 after hatching. The feeding levels applied to produce the irreversible starvation were fed control (FC), unfed control (UC), delayed first feeding for 1 (1DF), 2 (2DF) and 3 days (3DF). The whole body RNA/DNA ratio and the daily protein growth rate were individually analyzed. There were no survivors left in unfed group on day 6. Irreversible starvation (IS) occurred on the first day after first feeding which suggest the Black Sea anchovy larvae have a very low tolerance to starvation and the critical RNA/DNA ratio was 1.022 ± 0.20. The survival rate in the unfed control was similar to the other delayed groups. The highest daily protein growth rates were on day 6 with 43.45% for FC. Based on IS derived from RNA/DNA, 91% survival probability was detected in field-caught larvae. In future, irreversible RNA/DNA ratio can be used for monitoring and comparing of nutritional status and recruitment probability of different cohorts of the Black Sea anchovy larvae.

Food ingestion, prey selectivity, feeding incidence, and performance of yellowtail kingfish Seriola lalandi larvae under constant and varying temperatures

This study tested the effects of constant and varying temperatures on newly hatched yellowtail kingfish Seriola lalandi larvae in two experiments. In Experiment I, four constant temperatures (21, 23, 25, and 27 °C) were tested under fed or unfed conditions with the fish age from the day of hatch to 24 days post hatch (DPH). Temperatures at 25 and 27 °C reduced the time of fish to reach irreversible starvation, but did not affect the percentage of fish that were able to ingest food. Fish survivals at 21 and 23 °C were significantly higher than those at 25 °C by 24 DPH, but all fish died at 27 °C by 24 DPH in the treatment with food. In Experiment II, three constant temperatures (21, 23, and 25 °C) and two varying temperatures (21–23 and 21–25 °C) were compared using fish from hatch to 28 DPH. On 4 DPH, fish ingested more rotifers, but from 6 to 9 DPH, fish ingested fewer rotifers at 25 °C than at other temperatures. On 19 and 23 DPH, fish ingested more Artemia at 25 °C than at other temperatures. At 25 °C, fish selected for Artemia nauplii earlier than at other temperatures. Fish length and survival between constant temperatures (21 and 23 °C) were not significantly different, but fish survival at the constant 21 °C or at the 21–25 °C varying temperature was significantly higher than that at the constant 23 °C or at the 21–23 °C varying temperature. This study indicates that within the range of temperature tested, the optimal temperature for the first feeding larvae is 21–23 °C after hatch and mortality is likely to occur at ≥25 °C in the first 10 DPH, but fish grew faster at 25 °C after they adapted to the increasing temperature.

Thermal windows supporting survival of the earliest life stages of Baltic herring (Clupea harengus)

Abstract Peck, M. A., Kanstinger, P., Holste, L., and Martin, M. 2012. Thermal windows supporting survival of the earliest life stages of Baltic herring (Clupea harengus). – ICES Journal of Marine Science, 69: 529–536. Projecting climate-driven changes in marine systems will require knowledge on how thermal windows affect the vital rates of key species. To examine the potential, direct effect of climate-driven warming on southwest Baltic herring, we quantified the survival, development, and biochemical condition of embryos (eggs and yolk-sac larvae) at ten temperatures between 2.9 and 21.7°C. Viable hatch was highest from 7 to 13°C, <20% at 2.9°C and 0% at 21.7°C. Between 5 and 19°C, increasing temperature (T) decreased the time to 50% hatch (Ht, h,): Ht = 4461.9 × T − 1.24 (r2 = 0.98, p < 0.0001). Using degree-days [°d = T (°C) × age (d)] could normalize some (but not all) thermal effects. Most hatching occurred 90–120°d post-fertilization, unfed larvae lost 0.33 µg dry mass (DM) °d−1, larvae did not survive >160°d post-hatch. RNA–DNA ratios rapidly decreased between 50 and 80°d post-hatch, whereas DNA ×DM−1 increased throughout the yolk-sac phase and likely provides a stronger indicator of irreversible starvation. The critical, “mixed feeding” stage is likely 60–100°d post-hatch. The broad thermal tolerance of herring embryos makes “direct”, negative effects of warming unlikely; however, a lack of common methods among studies makes it difficult to project how climate warming will affect embryos of different fish populations and species.

Dynamics of chemical composition of the Black Sea gray mullet Mugil cephalus in the period of early ontogenesis and its dependence on temperature and salinity

Results of experiments on the study of the effect of temperature and salinity on dynamics of the chemical composition of gray mullet Mugil cephalus in the embryonic-larval period of development are presented. During the period of endogenous feeding (from the beginning of egg cleavage to transition of larvae to active feeding), lipids are spent with a greater rate than protein. After transition of larvae to exogenous feeding, an increase in the absolute concentration of proteins compared to lipids begins earlier and proceeds more intensively. The stage of irreversible starvation in larvae of gray mullet starts at a loss of 39–44% of protein and of the same amount of lipids of their initial content at the moment of hatching. Minimal protein losses over the period of embryonic development of gray mullet, as well as of protein and lipids towards the moment of termination of resorption of yolk sac, are observed in the range of temperatures of 21–25°C. Under conditions of low salinity (13–15‰) in the process of resorption of the yolk sac, lipids are spent more economically than at a higher salinity (17–19‰) at the expense of an increase in protein losses. Thus, a decrease in specific weight promoting the retention of buoyancy of larvae in water of low density is achieved.

Seasonal Differences in Biochemical Adaptation to Fasting in Juvenile and Subadult Steller Sea Lions (Eumetopias jubatus)

Nine Steller sea lions (Eumetopias jubatus) aged 1.75-6 yr were experimentally fasted for 7-14 d during the breeding and nonbreeding seasons to identify changes in plasma metabolites that are indicative of fasting and to determine whether the ability of sea lions to fast varies seasonally or with age. Although some animals approached the limit of their protein-sparing ability by the end of our fasting experiments, there was no sign of irreversible starvation biochemistry. Plasma blood urea nitrogen (BUN) concentrations decreased in all animals within the first week of fasting, reflecting a shift to a fasting-adapted state; however, significant increases in plasma BUN concentration at the end of the nonbreeding season fasts suggest that subadult Steller sea lions were not able to maintain a protein-sparing metabolism for a full 14 d during the nonbreeding season. In contrast, juveniles were able to enter protein sparing sooner during the nonbreeding season when they had slightly higher initial percent total body lipid stores than during the breeding season. Subadult and juvenile sea lions had low circulating ketone body concentrations compared with young sea lion pups, suggesting an age-related difference in how body reserves are utilized during fasting or how the resulting metabolites are circulated and catabolized. Our data suggest that metabolite concentrations from a single blood sample cannot be used to accurately predict the duration of fast; however, threshold metabolite concentrations may still be useful for assessing whether periods of fasting in the wild are unusually long compared with those normally experienced.

Early hatch: a strategy for safe downstream larval transport in amphidromous gobies

The downstream migration to sea of newly-hatched larvae of amphidromous fishes exposes them to the risk of irreversible starvation if migration takes too long. Some fishes, especially sicydiine gobies, exhibit early hatch of eggs, often less than 48 h after fertilisation, and the newly-hatched larvae are at a very early stage of ontogeny, with no functional mouth or fins, no functional eye, and little pigmentation in the eye or elsewhere. This may facilitate survival as it means that downstream migration takes place when plenty of yolk remains, minimising the risk of starvation. Additional behaviours, such as positive phototaxis, continual swimming up into the water column, and hatching during elevated river flows, may also have contributed to rapid downstream transport and survival.

Nutritional condition of Anguilla anguilla starved at various salinities during the elver phase

The effects of food deprivation and environmental salinity (<1, 10 and 20) on survival, fish morphology, organization of the digestive system and body lipid reserves in European eel Anguilla anguilla during the transition from glass eel to elver, were evaluated. Fasted elvers kept in fresh water were able to withstand starvation for >60 days, while those in brackish environments (salinity 10 and 20) reached the level of irreversible starvation at 37 and 35 days, respectively. The high level of lipid reserves contained in liver inclusions and the abdominal cavity (perivisceral deposits) in elvers might explain their long resistance to starvation and differences in fasting tolerance under different salinities. Fasting resulted in a significant reduction of the elvers’ condition factor and body depth. There were severe histopathological changes in the digestive system and musculature, such as the alteration of the liver organization, and hepatic glycogen and lipid content, shrinkage of enterocytes and reduction of their height, pancreas degeneration, autolysis of the oesophageal and intestinal mucosa and disarrangement of myofibrils and degeneration of trunk musculature. Degeneration of the oesophageal and intestinal mucosa as a consequence of fasting might have impaired digestive and osmoregulatory functions in feed‐deprived fish, directly affecting the tolerance to starvation and survival. Length of food deprivation was associated with a significant increase in mortality, coefficient of variation, cannibalism and point of no return at high salinities. Mortality was dependent on food deprivation and salinity concentrations. Environmental salinity directly influenced the ability of elvers to withstand starvation; once glass eels metamorphosed into elvers, they tolerated starvation better in fresh water than in brackish environments.

Feeding resumption, morphological changes and mortality during starvation in Japanese flounder larvae

Japanese flounder Paralichthys olivaceus larvae established first feeding 3 days after hatching (DAH) at c. 17° C. Non‐fed fish reached irreversible starvation at age 5 DAH. Non‐fed fish showed similar feeding rate and feeding intensity as the fed fish when they were provided with prey before 5 DAH, after which the starved larvae did not feed even when prey became available. None of the six morphological measurements examined (total length, body height, eye height, head height, gut height and myotome height) showed significant differences between the non‐fed and fed larvae until 5 DAH. Normal development continued only in the fed group, and the non‐fed larvae showed reverse growth or body collapse after 5 DAH. Owing to the shrinkage and collapse at the top of head due to starvation, head height could be a sensitive indicator of starvation in Japanese flounder larvae. In the fed treatments, high mortality occurred from first feeding (3 DAH) to irreversible starvation (5 DAH), accounting for about two‐thirds to three‐quarters of the overall mortality (46–52%) throughout the experiments. This mortality was not prey density or larval density dependent. Mortality during the same period in the non‐fed larvae accounted for about a third of the overall mortality (100%).

Impact of spectral composition on larval haddock, Melanogrammus aeglefinus L., growth and survival

In a small-scale culture experiment, larval haddock, Melanogrammus aeglefinus L., were raised under various combinations of light quality [blue (470 nm), green (530 nm) or full-spectrum white light] and light intensity [low (0.3–0.4 µmol s−1 m−2) or high (1.7–1.9 µmol s−1 m−2)], and in total darkness (both fed, and starved). Larval growth (0.9% day−1 in standard length; 2.4% day−1 in body area) was not significantly different between any combination of coloured light. At the time of total mortality in the starved treatment, survival was significantly reduced under low intensity, full-spectrum white light (13%) vs. all other coloured light treatments (68%). Larvae raised under both continuous dark treatments (fed and starved) exhibited morphological changes associated with irreversible starvation (point-of-no-return). Lack of a pronounced effect of light quality on larval haddock growth probably results from a combination of plasticity in early larval vision, and enhanced encounter rates between larvae and prey at the relatively high prey densities used in aquaculture.

Spatial distribution of ciliates, copepod nauplii and eggs, Engraulis japonicus post-larvae and microzooplankton herbivorous activity in the Yellow Sea, China

The abundance of anchovy Engraulis japonicus larvae, >20 mum ciliates, copepod eggs and nauplii, and microzooplankton herbivorous activity were studied in the Yellow Sea in June 2000. Anchovy juveniles and larvae were found in only 6 of the 19 stations sampled. The ciliate communities were dominated by 2 species: Laboea strobila and Strombidium compressum. In the surface waters, the abundance of L. strobila ranged between 0 and 560 ind. l(-1). S. compressum only appeared at Stns 15 to 18 (20 to 3300 ind. l(-1)). L. strobila was found mainly in the top 20 m. The abundance of L. strobila was less than 50 ind, l(-1) in waters deeper than 25 m. S, compressum showed subsurface abundance peaks at the salinity abnormality. Tintinnids occurred occasionally with abundance lower than 100 ind. l(-1), The total ciliate abundance fell in the range of 40 to 3420 ind. l(-1). The ciliate biomass in the surface water and the water column ranged between 0,15 and 6.76 mug C l(-1) and 0.4 and 134.4 mg C m(-2), respectively, In the surface waters, the abundance of copepod eggs and nauplii ranged from 0,3 to 3.1 and 1,1 to 15.6 ind, l(-1), respectively. The average abundance of copepod eggs and nauplii in 4 depth (0, 5, 10 and 20 m) fell in the range of 0.2 to 2.8 and 1.0 to 29.4 ind. l(-1), respectively. As a food item of the E. japonicus post-larvae, the abundance of copepod nauplii and eggs appeared to be low. The abundance peaks of ciliate and E, japonicus post-larvae coincided. Although not found in the gut of E, japonicus post-larvae, aloricate ciliates might be ingested by first-feeding anchovy larvae, preventing initial starvation and prolonging the time to irreversible starvation. On the basis of dilution experiments with positive microzooplankton grazing rates, microzooplankton grazed at rates of 0 to 0.61 d(-1). Grazing pressure of microzooplankton on chlorophyll a standing stock (P-i) and potential chlorophyll a primary production (P-p) were 17 to 46% and 35 to 109% d(-1), respectively.

Detecting growth in gilthead seabream, Sparus aurata L., larvae fed microcapsules

The ability to grow Sparus aurata fed a prototype microencapsulated food in relation to larval age was examined. The contribution of live prey in co-feeding experiments (live + inert food) was also determined. To attain these objectives several feeding regimes differing in the time that inert food was introduced were tested during the first 2 weeks of larval life. Larvae fed microcapsules alone from first feeding did not increase their dry weight during the experimental period, but after the point of irreversible starvation (day 8 after hatching), the larvae were able to grow (specific growth rate 0.034) and recover their initial dry weight. The larvae fed microcapsules from day 8 or day 12, after previously being fed rotifers (from day 4 to day 8 or 12), showed similar growth rates (specific growth rate 0.053 and 0.034, respectively), although in these cases the final dry weight was higher. Survival of larvae fed only microcapsules ranged from 11%, when the capsules were added from first feeding, to over 50% when pre-fed rotifers. The addition of live prey (5% of the total food supplied on dry weight basis) improved the survival (42%) when the microcapsules were supplied from the start of feeding. Feeding incidence on microcapsules was similar to that obtained with rotifers and the physiological status of the surviving larvae at end of the experiments was acceptable. Water quality was similar between the controls fed rotifers and the treatments fed microcapsules, indicating that no negative effect on larval growth could be attributed to water quality. This study indicates that S. aurata larvae are able to grow when fed only microcapsules, although with a low growth rate probably due to a lower assimilation of the diet. Further experiments testing other sources of protein and additives are needed in order to understand the factors that are limiting larval growth.

Aspects of the early life history of galjoenDichistius capensis

Laboratory experiments were conducted to determine the relationship between temperature and embryonic duration for fertilized galjoen eggs, and to examine the pattern of endogenous food utilization in early galjoen larvae. Embryonic duration decreased with increasing temperature, the relationship being best described by a power function with a negative slope. The lower lethal limit for developing eggs lay between 14 and 16°C. Newly hatched larvae rapidly exhaust their endogenous food reserves, the yolk sac being depleted at a slightly faster rate than the oil globule. Larvae approach first-feeding at 110 h after hatching at 18°C, and exhibit a short time period to irreversible starvation. Galjoen larvae appear to be particularly vulnerable to catastrophic starvation-induced mortality in nature.

Development, Survival, and Growth of Larval Weakfish at Different Prey Abundances

Abstract We reared larvae of weakfish Cynoscion regalis at different prey abundances in the laboratory (20.5°C). Larvae began to feed 52 h after hatching. When prey was withheld up to 72 h after larvae had the ability to feed, there was no increase in starvation-induced mortality. However, when prey was withheld more than 24 h, growth was significantly reduced. Times to yolk exhaustion (70 h posthatching) and irreversible starvation (168 h posthatching) were similar to those measured for other marine fishes reared at similar temperatures. We measured growth and mortality of 3–9-d-old larvae at prey abundances approximating those found in Delaware Bay and concluded that natural variations in prey abundance in systems such as Delaware Bay are sufficient to cause large variations in the growth rate of young weakfish larvae.

Food limited survival of larval razorback sucker, Xyrauchen texanus, in the laboratory

Razorback suckers in Lake Mohave, Arizona-Nevada, are suffering recruitment failure. Concomitantly, lake zooplankton levels are low and variable. We test, under laboratory conditions, the possibility that starvation is a cause of low recruitment. Razorback sucker larvae that were starved, received food too late, or were provided with insufficient food died between 20 and 30 d after hatching. Yolk absorption was at ∼ 8d after hatching, the critical period during which larvae must feed or most will die lies between ∼ 8 and 19d, and the point of irreversible starvation for individuals is between 19 and 23 d after hatching. Results support food-related mortality as a contributor to year-class failure of razorback sucker in Lake Mohave.

Effects of delayed feeding and temperature on the age of irreversible starvation and on the rates of growth and mortality of Pacific herring larvae

The time periods from exhausion of the yolk to the age of irreversible starvation for Pacific herring Clupea harengus pallasi larvae were 8.5, 7.0 and 6.0 d at 6°, 8° and 10°C, respectively. These periods are within the range perviously measured for Atlantic herring larvae and other temperature zone fish species; they are long compared to the periods for tropical species. The variation in the length of this period is due almost entirely to temperature; the natural logarithm of the time period from fertilization to irreversible starvation is highly correlated (r=0.91) with the mean rearing temperature for 25 species of pelagic marine fish larvae. The rates of growth and mortality, measured for 26 experimental populations of Pacific herring larvae reared at 6°, 8° and 10°C and ten ages of delayed first feeding, decreased and increased, respectively with increasing age of first feeding and increasing temperature. These rates, adjusted for the effects of rearing conditions, were compared with the rates for natural populations of herring larvae. Growth is generally faster in the sea than in experimental enclosures. Two of the eleven estimates of natural mortality rate were high enough to indicate possible catastrophic mass starvation. This is consistent with Hjort's critical period concept of year class formation and it suggests that mass starvation occurs in 18 to 36% of the natural populations of first feeding herring larvae.

Feeding, growth, and survival of Engraulis mordax larvae reared in the laboratory

Methods are described for the successful rearing of northern anchovy larvae (Engraulis mordax Girard) on cultured foods. Larvae were fed successively on the unarmored dinoflagellate Gymnodinium splendens, the veliger of the gastropod Bulla gouldiana, and nauplii of the brine shrimp Artemia salina. Rearing containers ranging in capacity from 4.5 to 510 l were tested; the smaller ones were found to be most useful for laboratory experimentation. Irreversible starvation occurred when E. mordax were denied food for more than 1.5 days after yolk absorption. Growth rates of larval anchovies fed different diets were compared. Larvae fed G. splendens grew for 1 week at the same rate as animals fed wild plankton, but did not maintain this rate. Laboratory survival of E. mordax larvae on a diet of G. splendens alone, did not differ significantly when veligers supplemented the diet. However, when G. splendens and veligers were fed simultaneously to E. mordax larvae, growth rate was greatly improved, although still not matching the growth attained on a diet of wild plankton. Length (L) versus weight (W) analyses were made for all larvae at all diets. The results showed that weight could be calculated most accurately from length by the relationship log W=3.3237 log L-3.8205, regardless of diet.