Dynamics of intracohort cannibalism in cultured fish

Abstract Cannibalism is a frequent phenomenon in fish, especially in culture environments where fish are unable to escape predation via habitat segregation or migration. Not all cultured fish species start to exhibit cannibalism at the same age or size, nor is cannibalism equally intense in different species or life stages. Predator to prey size ratios vary substantially between species and life stages, chiefly because cannibalism is governed by gape size limitations and allometric growth of mouthparts. The development of sense organs, hard body parts, swimming and escape capacities in both the predator and the prey also influence prey size selectivity. The dynamics of cannibalism are influenced by these, as well as by environmental, factors that have effects on feed intake, growth depensation and facilitate or complicate the displaying of cannibalistic behaviour. Knowledge about cannibalistic behaviour and the logistics of cannibalism along with environmental enhancement are prerequisites for the mitigation of cannibalism in aquaculture. Also, within the context of strain selection, it is of importance to determine whether cannibals are natural‐born killers or just lottery winners. These factors are discussed, chiefly as they apply to intracohort cannibalism. In addition, guidelines are suggested for cannibalistic risk assessment, and methods for mitigation of cannibalism are discussed.     

What causes cannibalization‐associated suffocation in cultured brown‐marbled grouper,Epinephelus fuscoguttatus (Forsskål, 1775)?

During culture of grouper, cannibalism is a frequent phenomenon that usually causes economic loss. Grouper culture often requires grading to prevent size‐dependent cannibalism. In comparison with orange‐spotted (Epinephelus coioides) and giant grouper (E. lanceolatus), failure to swallow prey during cannibalism is frequently observed in brown‐marbled grouper (E. fuscoguttatus). The cannibal cannot engulf the entire prey and the two fish ultimately end up dying together. Herein, we attempted to compare morphometric differences among orange‐spotted, giant and brown‐marbled grouper. We established a cannibal–prey total length (TL) relationship for brown‐marbled grouper: TL_prey=0.71 TL_cannibal−1.75. According to the equation, a difference of approximately 50% in TL is a threshold to use for grading the grouper. This value is much larger than that used (30%) in orange‐spotted and giant grouper, and this size difference results in a higher incidence of failed cannibalism attempts in brown‐marbled grouper. It is our belief that the standard grading method will fail to produce as good an effect in brown‐marbled grouper as is seen in orange‐spotted and giant grouper. Therefore, in addition to grading, other manipulations such as satiation feeding, nutritional supplementation and optimal stocking densities should be applied to reduce cannibalism of brown‐marbled grouper.     

Application of logistic regression analysis to predict cannibalism in orange‐spotted grouper Epinephelus coioides (Hamilton) fry

Cannibalism is frequently observed in larviculture of orange‐spotted grouper Epinephelus coioides. Previously, based on measurements of morphometric characters, a linear equation of total length (TL) of prey to cannibals was proposed: TL_prey = 0.80 TL_cannibal – 1.50. To verify the reliability of the equation, experiments were performed with pairs of fish with different TLs. Cannibalism occurred only when the cannibal‐prey size ratios were equal to or larger than that predicted by the equation. To predict the probability of cannibalism among the grouper of known TLs, a logistic regression model was proposed. The logistic regression model is: The logistic regression model showed the following: when either TL_prey or TL_cannibal is constant, the probability of cannibalism increases with increase in the cannibal‐prey size ratios; if given a constant cannibal‐prey size ratio, probability of cannibalism is lower in early stages than in later stages. The prediction contrasts with that calculated from the linear equation where the minimum cannibal‐prey size ratios decrease with size of the cannibal. However, the prediction matches observed rearing experiences: cannibals prefer smaller prey to larger ones and the cannibalism rate declines as fry age.     

A production season of turbot larvae Scophthalmus maximus (Linnaeus, 1758) reared on copepods in a Danish (56°N) semi‐intensive outdoor system

Turbot were reared from yolk sack larvae to juvenile in an outdoor semi‐intensive system. Three production cycles were monitored from May to September. A pelagic food chain was established with phytoplankton, copepods and turbot larvae. Abiotic and biotic parameters of lower trophic levels together with turbot larval survival, development, prey electivity and growth were monitored. A decreasing larval survival from 18.4% in May to 13.6% in July and just 7.0% in September was observed. The overall phytoplankton and copepod abundance decreased during the productive season. The turbot larval growth showed significant differences between larvae below (isometric) and above (allometric) 7 mm. Larval fish gut content showed no differences with available prey between production cycles. Therefore, it appears that the available prey concentration is governing their growth in this outdoor system. First‐feeding turbot larvae exhibited active selection for nauplii whereas developed larvae switched to copepodites and adult copepods. Although developing turbot larva exhibited active selection towards copepod size classes, there was no evidence of selective feeding on either of the two dominant copepod species. The turbot larvae's prey ingestion was modelled together with the standing stock of copepod biomass. The model results indicated that the estimated need for daily ingestion exceeded the standing stock of copepods. Hence, the initially established food web was unable to sustain the added turbot larvae with starvation as a consequence. We therefore suggest several solutions to circumvent starvation in the semi‐intensive system.     

Experimental evaluation of inorganic fertilization in larval giant grouper (Epinephelus lanceolatus Bloch) production

A major constraint in successful larviculture of groupers has been the small gape of the larvae and hence the requirement for small prey at first feeding. In this study, we examined how maintaining a phosphate concentration of 100 μg P L^?1 and an inorganic nitrogen (N) level of 700 μg N L^?1 via weekly fertilization with inorganic fertilizers affected phytoplankton, zooplankton and giant grouper larval survival in relation to a control group that was provided with rotifers immediately after larvae hatched. Unicellular algae, zooplankton within the size ranges of 10–50 μm and 50–100 μm and survival of giant grouper larvae were all significantly higher in the fertilized treatment compared with the control. Stomach analysis revealed that ciliates and flagellates were actively consumed by larval fish in the fertilized group, whereas few rotifers were consumed in the control. We conclude that the inorganic fertilization method provides high densities of suitable‐sized prey for larval groupers at the onset of exogenous feeding before they are able to consume larger, commercially available rotifers and copepods.     

Aggressive behaviour and cannibalism in greater amberjack,Seriola dumerili : effects of stocking density,feeding conditions and size differences

Aggressive behaviour, assessed by 24‐h observations, and survival rates, determined in a 2‐week rearing experiment, were examined in greater amberjack, Seriola dumerili, subjected to single and multiple factors (high density, restricted feeding and diverse size). Aggressive behaviour frequency in the group subjected to both restricted feeding and size diversity (FS) was significantly higher than that in the other groups (Tukey, n=4, P<0.05). In the FS group, aggressive behaviour increased with the starvation time from 19 days post hatching (dph) to 23 dph (two‐way analysis of variance, Tukey, n=4, P<0.05), but decreased gradually thereafter to 46 dph. In the rearing experiment, the survival rates for the diverse size and FS groups were lower than those of the control or restricted feeding groups (Kaplan–Meier, log‐rank test, n=100, P<0.01). Daily mortality in all groups was the highest at 24 dph; although dead fish were usually small, disappearance due to cannibalism was not observed during the rearing period. The results indicate that aggressive behaviour in greater amberjack is induced by hunger and size diversity in the early juvenile stages (23 dph). Mass mortality during seedling production was mainly caused by injury and the death of small fish due to aggressive behaviour/cannibalism.     

Ecological and Ethological Perspectives in Larval Fish Feeding

ABSTRACT

Low survival rates during larval stages constitute a major bottleneck in the successful culture of many marine and some freshwater fish. The availability of live food is recognized as a critical factor influencing larval survival. Live food is still superior to the best larval diets in terms of larval survival and growth. This paper reviews important ecological and ethological aspects of feeding, from hatching tothe weaning stage, and relates them to problems in larval culture. In general, freshwater fish larvae are easier to raise than marine fish larvae, because at hatching they are larger and endowed with more yolk reserves, are less sensitive to starvation, and canbe weaned to artificial diets sooner. The feeding behavior of the larvae can be analyzed in terms of the sequential components of predation: search, encounter, pursuit, attack, capture, and ingestion. The searching efficiency and encounter rates of the visual predator are influenced by prey parameters such as body size, conspicuousness, and evasiveness. Turbidity of the water and light intensity also affect prey detection. To changing prey densities, the larvae show typical Type II functional responses, which are influenced by prey handling time, which in turn is largely a function of prey size. Knowledge of larval functional responses is helpful in providing the right concentrations oflive food for larval culture. The larvae are initially gape-limited and exhibit prey size selectivity but gradually widen their prey size range as they grow. An aquacultural application of this is the commonly employed feeding protocol, prey size sequencing, in which progressively larger live food items are offered as the larvae grow. A thorough knowledge of the feeding behavior is also essential in the formulation of acceptable larval diets.     

Predation dynamics of mackerel on larval and juvenile anchovy: is capture success linked to prey condition?

We tested whether the predation dynamics of chub mackerel Scomber japonicus and spotted mackerel S. australasicus on young anchovy Engraulis japonicus relates to individual growth characteristics of the prey and could account for the growth-selective survival predicted by recruitment hypotheses. Juvenile and adult mackerel were sampled along with their young anchovy prey field in 2004 (juvenile mackerel and larval anchovy) and 2005 (adult mackerel and juvenile anchovy) off the Pacific coast of Honshu, Japan. The recent 5-day mean growth rate of larval and juvenile survivors and prey found in the stomach of mackerel was estimated from the otolith microstructure. No significant difference was found between the recent growth of larval or juvenile survivors and that of preyed individuals. We conclude that despite a relatively small body size, the high activity level and predation skills displayed by mackerel prevent fast-growing larvae and early juveniles from benefitting in terms of the expected survival advantage over slow-growers. Hence, growth-selective predation mortality of larval fish would depend on the feeding ecology of the predator rather than predator size. Selection for fast growth is more likely to occur under predation pressure from invertebrate organisms and small pelagic fish specialized on zooplankton, such as herring and anchovy.     

Morphological development and allometric growth of yellowtail kingfish Seriola lalandi V. larvae under culture conditions

Morphological development and allometric growth patterns of Seriola lalandi larvae were assessed to characterize normal growth patterns under culture conditions. Early ontogenetic stages of yellowtail kingfish exhibited an exponential growth in terms of standard length as a function of age. Five development stages were characterized from hatching to the juvenile stage: larval stage I (0–2 days post hatch, dph) with endogenous feeding, characterized by a small yolk sac, unpigmented eyes, primordial finfold surrounding the body and a closed mouth; larval stage II (2–15 dph) characterized by mouth opening, complete pigmentation of eyes and the beginning of the exogenous feeding; subsequently, in the larval stage III (15–25 dph) the posterior tip of notochord of the larvae bended upward and the first rays appeared in fins, concomitant with a change in swimming behaviour; thereafter, larval stage IV (post‐flexion stage; 25–30 dph) began when larvae resembled in morphology to a juvenile organism; however, caudal and dorsal fins were not completely development. Lastly, the juvenile stage was reached 30 dph characterized by a morphology and fin structures similar to those of the adults. Growth and development of structures and organs associated with vital functions such as feeding, sensorial and breathing systems seemed to be more critical previous to 23 dph, which was reflected with a positive allometric growth of head and eyes during this period. The results from this study can be used as a tool‐guide to assess normal development in larval research with S. lalandi to improve existing rearing protocols in hatchery production.     

Ontogenetic diet shifts of age-0 smallmouth bass (Micropterus dolomieu Lacepède) in the New River, West Virginia, USA

Larval and juvenile smallmouth bass (Micropterus dolomieu Lacepède; 8.5–85.0 mm total length (TL)) were collected from 2 sites in the New River, West Virginia, in the late spring and early summer to document diet shifts during early ontogeny. The first foods of smallmouth bass (TL = 9 mm) were primarily Chironomidae and microcrustaceans (primarily Copepoda). Other aquatic insects, primarily Ephemeroptera, became more abundant in the stomachs as TL increased. A shift in the proportions and types of prey consumed began at approximately 15 mm TL and was primarily attributed to fin development and increased mouth size. Foraging success, measured by number of prey per stomach, stomach fullness, and average prey volume was lower for first-feeding smallmouth bass than for later life stages. Mouth width appeared to restrict the size of prey consumed by larval smallmouth bass, but the maximum prey width never approached the mouth width for fish longer than 35 mm TL.     

Bioenergetics of cannibalism in juvenile barramundi Lates calcarifer (Bloch): exploring growth advantage of fish fed live prey and formulated diet

The present study investigated the growth performance of juvenile barramundi Lates calcarifer (Bloch) fed conspecific prey (CP), formulated diet (FD) and a mix of both (MIX) using a bioenergetics approach. Fish in the MIX treatment ingested significantly more CP than FD by dry mass. However, prey mass ingestion and cannibalism rate in the MIX treatment were significantly lower than in the CP treatment. This indicates that the provision of alternative food does not complete mitigate cannibalism, but it can significantly reduce cannibalism in barramundi. Fish in the FD treatment showed a significantly higher daily food intake than fish in the CP or MIX treatments. However, fish fed conspecifics showed significantly better feed conversion efficiencies, apparent digestibility rates and growth performances. Exclusive cannibalistic barramundi assimilated significantly more energy consumed, with 1.5% of energy lost in faeces comparing with 7.3% of siblings feeding exclusively on FD. Consequently, exclusive cannibals channelized more energy consumption into growth (57.1%) than those fed solely on FD (43.9%). Therefore, high energy allocation into growth promoted better feed conversion efficiency and growth performance of cannibalistic barramundi than siblings fed solely on FDs. This study implies that fast‐growing cannibals may continuously prey on slow‐growing conspecifics due to growth advantage through cannibalism. Therefore, size heterogeneity should be reduced at initial stocking and controlled as fish grow to avoid the emergence of new cannibals.     

Larviculture of the Greasy Grouper Epinephelus tauvina F. and the Brown-Marbled Grouper E. fuscoguttatus F. in Singapore

This paper reports the larviculture of two grouper species, the greasy grouper Epinephelus tauvina and the brown-marbled grouper E. fuscoguttatus , and examines the technical feasibility of breeding the fish. Fertilized eggs for larviculture were obtained by induced spawning through multiple hormonal injections of the female brooders, followed by artificial fertilization for the greasy grouper and by natural spawning in netcages for the brown-marbled grouper.
For both species, larviculture was divided into three operational stages, i.e., stage 1 (day 0–12), stage 2 (from day 12 to day 24 for the greasy grouper and to day 30 for the brown-marbled grouper) and stage 3 (day 24 or 30 to metamorphosis). Larvae were transferred to clean tanks after each stage. Total mortality around day 5–8 was common for the greasy grouper. Several modifications, including the feeding with super-small strain rotifers, intensive feeding of rotifers with Nannochloropsis and the use of an oil-skimmer, have been made to improve the situation. Two other major problems in larviculture were the high mortality observed after day 25 in the greasy grouper and the high cannibalism from day 35 onwards for the greasy grouper and from day 30 onwards for the brown-marbled grouper. The shock syndrome exhibited by both species during the periods made culling of the fish impossible.
Based on the spawning and larval characteristics, brown-marbled grouper is considered a better potential species for large scale fry production than the greasy grouper.     

Larval and juvenile Australian smelt Retropinna semoni somatic and otolith growth parameters – implications for growth interpretation of wild fish

Abstract –  Relationships between fish length, otolith size, age and weight were assessed for a population of wild Australian smelt ( Retropinna semoni ) larvae and juveniles captured over a 4-year period to aid further interpretation of growth and condition during the early life history of the species. Nonlinear smoothed generalized additive models best described the fish–otolith size relationship during the larval and juvenile period, indicating that the proportionality between fish length and otolith size varies in relation to size. It is proposed that back-calculated predictions of fish size at a previous age or otolith size, accounting for individual variation is possible by assuming a body proportional hypothesis. Growth rate of larval and juvenile Australian smelt was best described using the Gompertz model that indicated a steady decline in growth rate after around 30 days of age. The allometric growth of larval and juvenile Australian smelt established from the length/weight relationship can subsequently be used to assess the condition of fish within this population using a relative condition or relative weight condition index. The results of the study have provided significant information to enable more precise growth reconstruction and condition assessment for the species in Australian lowland rivers.     

Density‐ and size‐dependent mortality in fish early life stages

The importance of survival and growth variations early in life for population dynamics depends on the degrees of compensatory density dependence and size dependence in survival at later life stages. Quantifying density‐ and size‐dependent mortality at different juvenile stages is therefore important to understand and potentially predict the recruitment to the population. We applied a statistical state‐space modelling approach to analyse time series of abundance and mean body size of larval and juvenile fish. The focus was to identify the importance of abundance and body size for growth and survival through successive larval and juvenile age intervals, and to quantify how the dynamics propagate through the early life to influence recruitment. We thus identified both relevant ages and mechanisms (i.e. density dependence and size dependence in survival and growth) linking recruitment variability to early life dynamics. The analysis was conducted on six economically and ecologically important fish populations from cold temperate and sub‐arctic marine ecosystems. Our results underscore the importance of size for survival early in life. The comparative analysis suggests that size‐dependent mortality and density‐dependent growth frequently occur at a transition from pelagic to demersal habitats, which may be linked to competition for suitable habitat. The generality of this hypothesis warrants testing in future research.     

卵形鲳鲹仔稚鱼异速生长的研究

以传统的理论生物学研究方法,对孵化后卵形鲳鲹1~36日龄仔、稚鱼各器官测量和分析,研究其在早期环境适应上的异速生长及其生态学含义,以期为卵形鲳鲹的人工繁殖、育苗提供参考。试验结果表明,卵形鲳鲹仔、稚鱼的感觉、呼吸、摄食和游泳等器官快速分化,均存在异速生长现象。在头部器官中,吻长、口宽、眼径和头高在仔鱼期均为正异速生长,稚鱼期头高为等速生长,吻长、眼径和口宽为负异速生长。在身体各部位中,仔鱼期头长、体高和尾长为正异速生长,躯干长为负异速生长;稚鱼期各部分皆为等速生长;在游泳器官中,仔鱼期卵形鲳鲹胸鳍长、尾鳍高和臀鳍长为正异速生长,尾鳍长为等速生长,背鳍长为负异速生长;稚鱼期背鳍长和臀鳍长为正异速生长,胸鳍长、尾鳍长和尾鳍高为等速生长。卵形鲳鲹这些关键部位的快速发育,使外源性营养开始后以最小的代谢损耗获得了生存能力的显著提升,对适应复杂的生存压力具有重要的生态学意义。     

驼背鲈(Chromileptes altivelis)的胚胎发育及仔、稚、幼鱼形态观察

对驼背鲈(Chromileptes altivelis)的胚胎发育及仔、稚、幼鱼的形态特征进行了详细的观察与研究,描述了从受精卵到仔、稚、幼鱼各发育期的时间和形态特征变化。结果表明,在水温25-26℃、盐度30的海水中,受精卵历时27 h 25 min完成整个胚胎发育过程,经历从卵裂、囊胚、原肠、神经胚到肌节形成、各器官的逐渐形成、变化、完善等一系列的胚胎发育和变化过程;根据其卵黄囊消长情况、鳞片的覆盖状态、体色发生的不同变化以及第二背鳍和腹鳍的消长,将胚后发育分为仔、稚、幼鱼3个阶段。在水温22-26℃、盐度29-31、DO≥5 mg/L的条件下,2-3 d仔鱼卵黄囊消失,开口摄食;生长发育至31 d,仔鱼已变态进入稚鱼期;培育至57 d,稚鱼完成变态,成为幼鱼。第二背鳍棘和腹鳍棘的生长与收缩等石斑鱼类早期发育的共性生长特征及其体表特性体色变化特征为驼背鲈胚后发育过程中最明显的特征。     

Larval feeding behaviour of the endangered fish golden bubblebee goodeid, Allotoca dugesi, implications for conservation of an endangered species

Abstract To improve survival of cultured juvenile fishes, it is important to understand prey preferences and predation behaviour of fish larvae. In this study, the feeding behaviour and prey preference of Allotoca dugesi (Bean), a small fish species endemic to Mexico and currently threatened with extinction are presented. Three zooplanktonic prey, viz. Brachionus calyciflorus (Pallas) , Moina macrocopa (Goulden) and Daphnia pulex (Leydig) were tested. The mean size (standard length ± SE, mm) of the larvae ranged from 9.0 ± 0.1 mm at week 1 to 18 ± 2 mm at the end of the experimental period (8 weeks). The gape size (mean ± SE) increased from 0.125 ± 0.002 mm at the first week to 2.300 ± 0.361 mm by the eighth week. Capture success (capture/attack) ranged from 0.80 to 0.98 with Brachionus , 0.72–0.94 with Moina and 0.17–0.46 with Daphnia . Prey preference experiments were conducted using B. calyciflorus, M. macrocopa and D. pulex at a fixed ratio of 5 : 2 : 2 ind. mL⁻¹, respectively, and revealed a positive selection for rotifers and Moina , but avoidance of Daphnia . The results are discussed with reference to conservation efforts for Allotoca dugesi .     

Preservation-induced changes in morphometrics of fishes: influence on prey size-choice in juvenile walleye, Stizostedion vitreum (Mitchill)

Abstract– Juveniles of the Gulf coast population of walleye, Stizostedion vitreum , 22.4–89.9 mm SL ( n =111) shrank significantly in SL and throat diameter over 12 months after being fixed in 10% formalin for 1 week and preserved in 50% isopropyl alcohol thereafter. Significant changes in body depth and total length (TL) were also determined for select larval fish prey that juvenile walleye might encounter in nature. The relationship between fresh SL and throat diameter in juveniles of the Gulf coast population of walleye (22.4–172.4 mm SL) is: throat diameter (mm) =−0.8783 + 0.0786 SL (mm) ( r ²= 0.988, P < 0.0001, n = 135). In laboratory experiments on prey size choice, walleye selected available prey near or less than their mean throat diameter, although several larger prey (7.4% of total) were also consumed. To determine the actual spectrum of prey sizes available to juvenile piscivores, we must adjust the realized size of the predator and prey for changes caused by preservation. Preservation-induced alterations in morphology translated into errors in the perceived pattern of prey size choice in walleye. The preservation-induced changes documented in this study, which are also supported by a number of other empirical data sets, must be included when modeling the relationships between feeding ecology, morphology, growth, and ecologically relevant indices (condition factors, relative weights, etc.).     

Differential growth rates related to initiation of piscivory by hatchery-reared larval Pacific bluefin tuna Thunnus orientalis

Fast growth plays an important role in survival processes during the early life stages of both field-captured and hatchery-reared Pacific bluefin tuna Thunnus orientalis. Marked growth variations in hatchery-reared tuna larvae are frequently observed even for the same age and within the same rearing tank after the onset of the piscivory. We hypothesized that these small growth variations in the growth of tuna larvae at the onset of piscivory lead subsequently to large growth variations and tested the hypothesis using three size groups (large, intermediate and small) of hatchery-reared fish by nitrogen stable isotope and otolith analyses. Stable isotope analysis revealed that the large group rapidly utilized prey fish larvae, but the smaller groups depended more on rotifers as the main prey item relative to the large group. The otolith radius from the core to the increment corresponding to the first feeding on yolk-sac larvae was compared among the three size groups. The results revealed that the large group had larger otolith radii than the small and intermediate groups. Our findings suggest that small growth variations apparent during the early larval stage of tuna could induce further large growth variations in the late-larval and juvenile stages through differences in the initial ability to utilize piscivory.     

Intra‐cohort cannibalism in early life stages of pikeperch

Cannibalism has been described in 390 teleost fish species belonging to 104 families. In rearing conditions, intra‐cohort cannibalism is one of the major bottlenecks during the early life stages of pikeperch (Sander lucioperca). This study aims to describe precisely the occurrence and the onset of cannibalism of this species during the first two post‐hatching months. In a first step, the cannibalistic behaviour was analysed through observations in three experiments. In each experiment, the number of cannibalistic cases was similar. From 14 to 48 days post‐hatching (dph), more than 60 % of prey ingestions were realized by tail‐first, but after 48 dph, the number of prey ingestions by head‐first increased. In a second step, the behavioural sequence exhibited to attack and to capture a conspecific was analysed, taking into account the size ratio between the cannibal and its prey. The behavioural sequence to capture was always the same, similar to a predatory sequence and it seems that the cannibal chose its prey about 10 s before attacking. Moreover, prey choice by a cannibal was based more on the size ratio between the cannibal and its prey than the previous activity of the potential prey. These new results could lead to solutions to decrease cannibalism in pikeperch rearing.