Energetic consequences of an inducible morphological defence in crucian carp

Crucian carp (Carassius carassius) increases in body depth in response to chemical cues from piscivores and the deeper body constitutes a morphological defence against gape-limited piscivores. In the field, deep-bodied individuals suffer a density-dependent cost when competing with shallow-bodied conspecifics. Here, we use hydrodynamic theory and swimming respirometry to investigate the proposed mechanism underlying this effect, high drag caused by the deep-bodied morphology. Our study confirms that drag is higher for deep-bodied crucian carp, both in terms of estimated theoretical drag and power curve steepness. However, deep-bodied fish swimming at the velocity associated with minimum cost of transport, U _mc, did not experience higher costs of transport than shallow-bodied fish. Deep-bodied crucian carp had significantly lower standard metabolic rates, i.e. metabolic rates at rest, and also lower U _mc, and the resulting costs of transport were similar for the two morphs. Nevertheless, when deep-bodied individuals deviate from U _mc, e.g. when increasing foraging effort under competition, their steeper power curves will cause substantial energy costs relative to shallow-bodied conspecifics. Furthermore, there is evidence that reductions in standard metabolic rate incur costs in terms of lower stress tolerance, reduced growth rate, and life history changes. Thus, this work provides links between hydrodynamics, a cost-reducing mechanism, and a density-dependent fitness cost associated with an inducible defence. Received: 22 March 1999 / Accepted: 14 June 1999     

Predator-induced morphology enhances escape locomotion in crucian carp

Fishes show a remarkable diversity of shapes which have been associated with their swimming abilities and anti-predator adaptations. The crucian carp (Carassius carassius) provides an extreme example of phenotypic plasticity in body shape which makes it a unique model organism for evaluating the relationship between body form and function in fishes. In crucian carp, a deep body is induced by the presence of pike (Esox lucius), and this results in lower vulnerability to gape-limited predators, such as pike itself. Here, we demonstrate that deep-bodied crucian carp attain higher speed, acceleration and turning rate during anti-predator responses than shallow-bodied crucian carp. Therefore, a predator-induced morphology in crucian carp enhances their escape locomotor performance. The deep-bodied carp also show higher percentage of muscle mass. Therefore, their superior performance in escape swimming may be due to a combination of higher muscle power and higher thrust.     

Predator recognition and defence strategies in crucian carp, Carassius carassius

Crucian carp from populations that lack piscivores are extremely vulnerable to predation. However, in the presence of piscivores these fish develop an inducible morphological defence, a deep body. This switch from a vulnerable, shallow-bodied morph to a morphologically defended morph makes this species very suitable for investigations of anti-predator strategies, and trade-offs between morphological and behavioural defences. To address these questions, we performed eight different experiments. We found that crucian carp exhibited fright responses to chemical cues from unfamiliar predators (northern pike, perch) when these were fed prey that contained alarm substance (for northern pike: crucian carp, roach; for perch: crucian carp). Cues from small pike that were fed prey that lacked alarm substance (swordtails) caused no significant fright response whereas cues from larger pike with the same diet did. Perch on a chironomid diet elicited weaker but significant fright responses. Starved predators caused as strong fright reactions as recently fed ones did, whereas no response was exhibited towards nonpredatory fish (roach, crucian carp). Crucian carp were able to detect the presence of pike after cues had been diluted to an equivalent of 21 000 l, and larger predators elicited stronger fright responses. Prior experience of predators decreased fright responses. In particular, individuals from populations that coexisted with northern pike responded less to chemical cues from northern pike than individuals without prior experience did. Thus, crucian carp may use both alarm-substance related and predator-related cues to identify predators. Further, they were able to discriminate between large and small predators. Finally, individuals from populations that coexist with predators exhibit less pronounced fright responses. These fish have an induced morphological defence, a deep body, which most likely decreases the need for strong antipredator behaviour.     

Phenotypic plasticity and predator effects on morphology and physiology of crucian carp in nature and in the laboratory

Crucian carp Carassius carassius show great phenotypic plasticity in individual morphology and physiology, and strong variation in population density in different fish communities. Small fish with shallow bodies and large heads are typical in overcrowded monospecific fish communities in small ponds, whereas deep-bodied, large fish are found in larger, multispecies lakes. Crucian carp are especially vulnerable to predation by piscivorous fish and their greater relative body depth in multispecies fish communities has been proposed to be an induced defence against size-limited predation, and hence to be an adaptive feature. Data are presented here on the two divergent body forms in field populations in eastern Finland, together with results of laboratory experiments on predator effects on morphology and physiology (growth, respiration, heart rate). The deep body can be achieved in a few months by introducing a low population density of shallow-bodied fish into a food-rich environment with no piscivores. In the laboratory, both the presence of piscivores (chemical cues) and enhanced food availability increased the relative depth of crucian carp, but only to a modest extent when compared to natural variation. It is concluded that the deep-body form of crucian carp in the low density populations of multispecies fish communities is the normal condition. Reproduction in monospecific ponds results in high intraspecific competition, low growth rate and a stunted morphology. According to pilot tests, the mechanism behind the predator effect in the laboratory might be a behavioural reaction to chemical cues (alarm substances/predator odour) causing changes in energy allocation: predator-exposed crucian carp adopt a 'hiding' mode with decreased activity (less swimming, lower respiration and heart rate) and with higher overall growth. Whether, and to what extent, this predator-induced mechanism works in nature is unclear.     

Interactions between predator- and diet-induced phenotypic changes in body shape of crucian carp

Predator cues and diet, when studied separately, have been shown to affect body shape of organisms. Previous studies show that the morphological responses to predator absence/presence and diet may be similar, and hence could confound the interpretation of the causes of morphological differences found between groups of individuals. In this study, we simultaneously examined the effect of these two factors on body shape and performance in crucian carp in a laboratory experiment. Crucian carp (Carassius carassius) developed a shallow body shape when feeding on zooplankton prey and a deep body shape when feeding on benthic chironomids. In addition, the presence of chemical cues from a pike predator affected body shape, where a shallow body shape was developed in the absence of pike and a deep body shape was developed in the presence of pike. Foraging activity was low in the presence of pike cues and when chironomids were given as prey. Our results thereby suggest that the change in body shape could be indirectly mediated through differences in foraging activity. Finally, the induced body shape changes affected the foraging efficiency, where crucians raised on a zooplankton diet or in the absence of pike cues had a higher foraging success on zooplankton compared to crucian raised on a chironomid diet or in the presence of pike. These results suggest that body changes in response to predators can be associated with a cost, in terms of competition for resources.     

Body morphology of crucian carp Carassius carassius in lakes with or without piscivorous fish

Crucian carp Carassius carassius was sampled during 1993 and 1994 in 21 lakes and ponds in east Norway In 10 of these lakes and ponds no piscivorous fish species was present, and in the remaining 11 lakes and ponds predators such as perch Perca fluvtalilis. pike Esox lucius, and trout Salmo trutta were common In general, crucian carp was larger in the lakes with predators than in those without predators The relative body depth (body height/body length) of crucian carp was significantly deeper in populations sympatric with predators (mean 0 358), compared to allopatric populations (mean 0 286) The variation in relative body depth was larger among the sympatric populations than among the allopatric populations The observed difference in relative body depth may be due to 1) predator induced changes m body morphology, 2) increased growth rates in lakes containing predator due to reduced intraspecific competition, and 3) size-selective predation     

Pugnose eels, Simenchelys parasiticus (Synaphobranchidae) from the heart of a shortfin mako, Isurus oxyrinchus (Lamnidae)

The body depth of crucian carp, Carassius carassius, increases in the presence of predator fish, thereby decreasing the vulnerability of crucian carp to predation. This phenotypic change is mediated by chemical signals, and is believed to result from a piscivorous diet of predators. We have shown that exposure to a piscivorous predator is insufficient to induce growth changes in crucian carp, since water from northern pike, Esox lucius, fed Arctic charr, Salvelinus alpinus, does not induce a change in crucian carp morphology, while water from pike fed crucian carp does. The determining factor is a chemical signal from the skin of crucian carp, as demonstrated by exposure to skin extracts from conspecifics. We suggest that alarm substances from conspecifics, expressing primer pheromone effects, are the most likely candidates for induction of the phenotypical changes.     

Trading off safety against food: state dependent habitat choice and foraging in crucian carp

The influence of hunger level and predation risk on habitat choice and foraging in crucian carp, Carassius carassius, were studied in a laboratory experiment. Experiments were carried out in aquaria with or without a predator (pike, Esox lucius). Habitat use and foraging activity of three-fish foraging groups of either fed or hungry crucian carp were studied. Fish were allowed to choose between an open (risky) habitat with Tubifex worms and a habitat with dense vegetation (safe) without food. Habitat use was significantly affected by both risk of predation and hunger level. Crucian carp spent less time in the open habitat when there was a predator present and they also spent less time there when fed than when hungry. Furthermore, there was a significant interaction between risk of predation and hunger level, indicating a state-dependent trade-off between food acquisition and predator avoidance.     

Phenotypic variation and associated predation risk of juvenile common carp Cyprinus carpio

Juvenile common carp Cyprinus carpio were collected from 10 lakes with variable predator abundance over 4 months to evaluate if morphological defences increased with increasing predation risk. Cyprinus carpio dorsal and pectoral spines were longer and body depth was deeper when predators were more abundant, with differences becoming more pronounced from July to October. To determine if morphological plasticity successfully reduced predation risk, prey selection of largemouth bass Micropterus salmoides foraging on deep- and shallow-bodied C. carpio was evaluated in open and vegetated environments. Predators typically selected deep- over shallow-bodied phenotypes in open habitats and neutrally selected both phenotypes in vegetated habitats. When exposed to predators, shallow-bodied C. carpio phenotypes shoaled in open habitat, whereas deep-bodied phenotypes occupied vegetation. Although deep-bodied phenotypes required additional handling time, shallow-bodied phenotypes were more difficult to capture. These results suggest that juvenile C. carpio gradually develop deeper bodies and larger spines as predation risk increases. Morphological defences made it more difficult for predators to consume these prey but resulted in higher vulnerability to predation in some instances.     

Consumption of crucian carp (Carassius carassius L., 1758) by restocked pike (Esox lucius L., 1758) in a lake with frequent winter hypoxia

To assess the effects of stocked pike (Esox lucius L.) on crucian carp (Carassius carassius L.) biomasses, the annual consumption of pike was estimated and compared with removal fishery catches. The studied lake, Lake Savijärvi, is a small (40 ha), shallow and eutrophicated lake in southern Finland with frequent algal blooms during summers and fish kills during winters. Until the 1980s, the fish fauna consisted of pike, perch (Perca fluviatilis L.), roach [Rutilus rutilus (L.)], crucian carp, and tench (Tinca tinca L.). Since 2003, when crucian carp were abundant in the extreme and with only a few roach and tench individuals, the lake has been biomanipulated by removal seining. To enhance the effects of seining, piscivorous pike were restocked in the spring of 2008. During the 3‐year study, the catch of crucian carp decreased from 243 to 136 kg while the catch of pike increased from 0.1 to 5.7 kg per seining hectare due to their spawning in the lake as of 2009. The total crucian carp consumption by captured pike was 588 kg during the 2008–2010 study period. When applying the number of pike estimated with the mark‐recapture method, consumption estimate increased to 917 kg, or 22.9 kg per lake hectare in 2010. Thus, pike consumption of crucian carp was about 17% of the removal catch in 2010.     

An experimental study of body size and food size relations in crucian carp,Carassius carassius

Synopsis In dense, single-species assemblages of crucian carp, competition is intense and results in populations of stunted fish. To explore mechanisms underlying this competition, we measured handling times, return rates, and prey choice for five sizes of crucian carp feeding on six sizes of a standardized food. Handling times increased with prey size and decreased with fish size. Return rates (dry mass ingested per unit handling time) increased dramatically with fish size, and generally decreased with increasing prey size, especially for small fish. Patterns of return rates among size-classes suggested that one or more size-related shifts in feeding efficiency exist for crucian carp; combined with physiological stresses related to winter anoxia, the inability of fish to make these shifts may contribute to size structures observed in high-density populations. Comparisons of relations among fish size, prey size, and return rates for crucian carp and bluegill, Lepomis macrochirus, suggest that similar intraspecific competitive relations exist between generalist species with size-structured populations. Despite differences in return rates among prey sizes, the extent of food selectivity based on prey size exhibited by crucian carp in two types of choice trials was less than predicted. Crucian carp commonly take in several items before mechanically processing food with their pharyngeal apparatus; this multiple prey processing may contribute to disparities between observed choice patterns and those predicted based on return rates for single prey.     

The Diel Activity of Crucian Carp, Carassius Carassius, in Relation to Chemical Cues from Predators

Chemical cues from piscivorous fish and prey alarm substances often cause rapid fright responses in prey. However little is known of how piscivore-related chemical cues affect prey behaviour over periods longer than a few hours. Here we have investigated how chemical cues from piscivorous northern pike, Esox lucius, affect habitat choice and diel activity of crucian carp, Carassius carassius, over an extended period 11 days. At the beginning of the experiment control fish were nocturnal while fish in the pike cue treatment were aperiodic. After 11 days, control fish had become more strongly nocturnal and displayed two activity peaks during early and late night whereas fish in the pike cue treatment were still aperiodic with no activity peaks. Habitat choice was aperiodic in both treatments throughout the experiment. In both treatments, more fish were found in the vegetation zone than in the open habitat. This was most pronounced when pike cues were present. These results demonstrate that short-term anti-predator responses to chemical cues from predators can translate into long-term adjustments of diel periodicity. Further, the results did not support the idea that crucian carp should switch to nocturnal activity in response to visually hunting predators. Control fish were nocturnal and chemical cues from pike did not make this pattern more pronounced.     

鲫鱼汤对阿霉素肾病大鼠Th17细胞相关炎性因子表达的影响

目的研究鲫鱼汤对阿霉素肾病大鼠IL-17、IL-23、IL-1β和CXCR2等表达的影响,探讨其治疗作用和机制。方法成年Wistar雄性大鼠40只,随机分为鲫鱼汤组、厄贝沙坦组、肾病组、空白对照组,除空白对照组,其他三组给予尾静脉注射6.2 mg/kg体重阿霉素建立肾病模型,空白组注射等容量生理盐水。模型成功后,给予鲫鱼汤灌胃干预9周,每周检测12 h尿蛋白定量,检测终末血生化指标变化,光镜下观察大鼠肾脏病理改变,免疫组化检测IL-17、IL-23、IL-1β和CXCR2在肾脏的表达,ELISA法检测IL-17、IL-23和IL-1β在血液中的含量。结果鲫鱼汤组大鼠血白蛋白水平高于肾病组(P=0.03)低于空白组(P=0.01);鲫鱼汤组大鼠肾组织IL-17、IL-23、CX-CR2较肾病组表达减少(P=0.01,P=0.01,P=0.02),较空白组表达增多(P=0.04,P=0.007,P=0.05)。结论 Th17细胞相关炎性因子增多是阿霉素肾病大鼠的发病机制之一,鲫鱼汤可通过升高血白蛋白,降低IL-17、IL-23、CXCR2表达而发挥肾脏保护作用。     

Using accelerometry to quantify prey attack and handling behaviours in piscivorous pike Esox lucius

Accelerometer technology was used to evaluate behaviours in the teleost ambush predator pike Esox lucius foraging on crucian carp Carassius carassius. Automated rule‐based estimates of prey‐size determined handling time were obtained and are compared with video‐recorded behaviours. Solutions to tag attachment and the limitations imposed by battery‐time and data‐logging capacities are evaluated.     

Antipredator phenotype in crucian carp altered by a psychoactive drug

Predator‐inducible defenses constitute a widespread form of adaptive phenotypic plasticity, and such defenses have recently been suggested linked with the neuroendocrine system. The neuroendocrine system is a target of endocrine disruptors, such as psychoactive pharmaceuticals, which are common aquatic contaminants. We hypothesized that exposure to an antidepressant pollutant, fluoxetine, influences the physiological stress response in our model species, crucian carp, affecting its behavioral and morphological responses to predation threat. We examined short‐ and long‐term effects of fluoxetine and predator exposure on behavior and morphology in crucian carp. Seventeen days of exposure to a high dose of fluoxetine (100 µg/L) resulted in a shyer phenotype, regardless of the presence/absence of a pike predator, but this effect disappeared after long‐term exposure. Fluoxetine effects on morphological plasticity were context‐dependent as a low dose (1 µg/L) only influenced crucian carp body shape in pike presence. A high dose of fluoxetine strongly influenced body shape regardless of predator treatment. Our results highlight that environmental pollution by pharmaceuticals could disrupt physiological regulation of ecologically important inducible defenses.     

Comparison of mouth morphology and prey size selection among three esocid taxa

Aquatic organisms, especially fishes, exhibit exceptional diversity in mouth morphology and this variation has been shown to influence foraging patterns. We compared mouth morphology among muskellunge Esox masquinongy, northern pike Esox lucius and their hybrid, tiger muskellunge E. masquinongy x E. lucius. Head and mouth size among the three taxa were similar for juveniles (<400 mm total length), but diverged with increasing length, being greater for northern pike than muskellunge. Tiger muskellunge had a head and mouth size intermediate to the two, but more similar to northern pike than muskellunge. Morphological differences among taxa were related to data examining prey size selection in laboratory and field experiments. In the laboratory, northern pike selected prey that were smaller than their maximum mouth width (widest point between outside corners of mouth), tiger muskellunge selected larger prey, and muskellunge size-selection was intermediate between the other two taxa. Among the three esocids, muskellunge had the smallest increase in handling time with increasing prey body depth relative to predator mouth width. In a common garden field experiment in three lakes containing mainly deep-bodied prey, results generally followed morphological patterns, with northern pike selecting larger prey compared to muskellunge. Although morphology predicted most of the variation in greatest body depth of prey consumed, the best predictor of prey size was a model that included predator mouth width, taxon, and interaction. Information comparing prey size selection among esocid taxa is useful for understanding how to manage esocid populations based on system-specific prey characteristics and also for understanding how variations in morphological characteristics of apex predators can influence prey vulnerability and ecosystem structure.     

Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory

The northern pike ( Esox lucius ) is a selective and important predator in lake ecosystems. Prey size in pike is limited by pike gape size, which is a linear function of pike body length. Here we show that the absolute gape-size limit in pike is greater than previously considered, and that maximum ingestible prey size is limited by prey body depth. Further, we experimentally show that pike prefer shallow-bodied roach before deeper-bodied common bream, and small prey sizes within each prey species. Handling time in pike increases with prey body depth, and since common bream are deeper-bodied than roach, handling time is longer for bream than for roach of the same length, but equal considering body depth. Prey handling time is suggested to be a major cost to the pike, since it increases the risk of losing the prey, as well as exposure to predation, kleptoparasitism and cannibalism. Consequently, prey vulnerability is determined by risk of predation and intraspecific interactions, and behavioural preferences in the pike, and not by pike gape-size limits. The consequences for natural populations is evaluated by analysing size structures of predator and prey fish populations in a eutrophic lake.     

Genetic diversity analysis of crucian carp (Carassius auratus) based on cyt b and D-loop-containing region around Hongze Lake

Environmental Biology of Fishes - Crucian carp (Carassius auratus) is an important freshwater aquaculture species in China. The study of the genetic diversity of native crucian carp will provide...     

Challenging fear: chemical alarm signals are not causing morphology changes in crucian carp (<Emphasis Type="Italic">Carassius carassius</Emphasis>)

Crucian carp develops a deep body in the presence of chemical cues from predators, which makes the fish less vulnerable to gape-limited predators. The active components originate in conspecifics eaten by predators, and are found in the filtrate of homogenised conspecific skin. Chemical alarm signals, causing fright reactions, have been the suspected inducers of such morphological changes. We improved the extraction procedure of alarm signals by collecting the supernatant after centrifugation of skin homogenates. This removes the minute particles that normally make a filtered sample get turbid. Supernatants were subsequently diluted and frozen into ice-cubes. Presence of alarm signals was confirmed by presenting thawed ice-cubes to crucian carp in behaviour tests at start of laboratory growth experiments. Frozen extracts were added further on three times a week. Altogether, we tested potential body-depth-promoting properties of alarm signals twice in the laboratory and once in the field. Each experiment lasted for a minimum of 50 days. Despite growth of crucian carp in all experiments, no morphology changes were obtained. Accordingly, we conclude that the classical alarm signals that are releasing instant fright reactions are not inducing morphological changes in this species. The chemical signals inducing a body-depth increase are suspected to be present in the particles removed during centrifugation (i.e., in the precipitate). Tissue particles may be metabolized by bacteria in the intestine of predators, resulting in water-soluble cues. Such latent chemical signals have been found in other aquatic organisms, but hitherto not reported in fishes.     

Male mate choice in the gynogenetic–sexual complex of crucian carp,<Emphasis Type="Italic"> Carassius auratus</Emphasis>

The asexual all-female Japanese crucian carp, Carassius auratus langsdorfii (Teleostei: Cypriniformes), reproduces gynogenetically, relying on the sperm of males of the sexual "host," C. auratus subspp. Theoretically, frequency-dependent mating preference of males to conspecific females can lead to the coexistence of asexual and sexual fish, if all else is equal. Our specific questions are whether males prefer conspecific females over asexual females and whether individuals show dominance hierarchies that potentially cause frequency-dependent mating preference. In an individual choice experiment, a tank was partitioned into three compartments with the middle one for a single male and the two outer ones for a sexual and an asexual female. The males of C. auratus bürgeri demonstrated a significant preference for ovulated conspecific females over ovulated asexual females. In contrast, in a group mating experiment, a single experimental tank included two males, a sexual female, and an asexual female together, and males chased and mated with both asexual and sexual females equally. Male mate preference was weak in group mating, which is typical in natural populations. Males and females of crucian carp showed no apparent agonistic behavior to each other in the group mating experiment. This is different from other gynogenetic complexes with the dominance hierarchy of males showing strong frequency-dependent mating preference (e.g., Poeciliopsis). We conclude that male mate preference is unlikely to be a strong frequency-dependent force maintaining the coexistence of asexual–sexual complexes of Japanese crucian carp. Received in revised form: 5 February 2001 Electronic Publication