Feeding ability and survival during starvation of marine fish larvae reared in the laboratory

The larvae of Clyde and Baltic herring (Clupea harengus L.), cod (Gadus morhua L.) and flounder (Platichthys flesus L.) were reared and fed to examine the changes in feeding ability and survival during progressive starvation. The time to initial feeding for yolk-sac larvae and to the point-of-no-return (PNR, when 50% of the larvae, although still alive, are no longer strong enough to feed) for both yolk-sac and older larvae were determined. The yolk-sac larvae of Clyde and Baltic herring, cod and flounder begin to feed on days 6, 3, 5 and 6 post-hatching at rearing temperatures of 7.5, 9.2, 6.9 and 9.5°C, respectively. The time to reach the PNR for yolk-sac larvae of these species is only 3–5 days after yolk resorption. From the onset of starvation in older larvae the time to reach the PNR is 6–7 days for 36-and 60-day-old Clyde herring at 9.6 and 10.5°C and for 46-day-old Baltic herring at 13.1°C but it is 23 days for 32-day-old flounder at 12.3°C. In yolk-sac larvae the peak of feeding rate and intensity usually occurred on the day that the yolk became exhausted, or 1 day later. Older larvae could withstand longer periods without food than yolk-sac larvae, especially in flounder. While the feeding rate during starvation of older larvae slowly decreased the feeding intensity first increased significantly and then decreased. Survival of larvae remained high up to the PNR.     

Effects of size on predation risk,behavioural response to fish,and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata)

Summary We used laboratory studies to examine the role of predation risk and cost of anti-predator behaviour in determining the behavioural response of several larval instars of Ischnura verticalis to a fish predator (Lepomis gibbosus). Smaller larvae were less susceptible to fish predation than larger larvae. Smaller larvae depressed movement to a greater degree in the presence of fish than did larger larvae; large larvae were generally less active than small larvae regardless of fish presence. Reduced feeding resulted in smaller larvae suffering more in terms of reduced growth than did large larvae. In general, our results tend to support the hypothesis that individuals that suffer high costs of anti-predator behaviour but little risk of predation may only exhibit anti-predator behaviours in the presence of predators, whereas individuals with a higher risk of predation and a lower cost of anti-predator behaviour may evolve anti-predator mechanisms that are in effect even in the absence of predators.     

The effect of invertebrate and vertebrate predators on the foraging movements of Ischnura elegans larvae (Odonata: Zygoptera)

SUMMARY.

• 1 The foraging movements of late instar Ischnura elegans larvae were monitored in laboratory experiments to study the effects of predators on larval feeding behaviour.
• 2 Ischnura larvae are sit-atid-wait, or ambush, foragers, moving occasionally between perches in search of profitable feeding sites. Larval foraging movements, monitored at different densities of Daphnia prey, increased significantly when prey were absent.
• 3 In experiments without prey, larval movement was inhibited by the presence of fish predators, as well as by invertebrate predators (Notonecta glauca), but not by closely related, non-predatory invertebrates (Corixa punctata) or physical disturbance of the water (intermittent air bubbles).
• 4 Further experiments varied Ischnura hunger levels (0–8 days without food) and illumination (light or dark) with and without notonectid predators. Hunger had no consistent effect on penultimate instar behaviour but final instar foraging activity was significantly modified: movements increased after 4 days starvation and decreased again after 8 days. This response was suppressed by the presence of predators. Both larval instars moved significantly less often in the light, even when predators were absent.
• 5 These phenotypically flexible predator-avoidance responses are likely to decrease the risk of predation by both visual and tactile predators. However, predators clearly have an important influence on the feeding niche of Ischnura larvae, and may decrease the overall feeding efficiency, growth rate, and survival of larvae by constraining their movement in search of profitable feeding sites.

     

Behavioral responses to fish kairomones and autotomy in a damselfly

The threat-sensitivity hypothesis predicts that prey species assess and adjust their behavior in accordance with the magnitude of the threat posed by a predator. A largely overlooked characteristic of a prey that will affect its sensitivity to predators is its history of autotomy. We studied threat-sensitive behavior to fish kairomones in larvae of Ischnura elegans damselflies, which had undergone autotomy, from a fishpond and from a fishless pond. In agreement with their higher perceived risk, larvae from the fishpond showed fewer rigid abdomen bends, foraged less and walked more slowly than larvae from the fishless pond. In line with their higher vulnerability to predators, larvae without lamellae spent less time foraging than larvae with lamellae. There was a decrease in swimming activity in the presence of fish kairomones except for larvae with lamellae from the fishless pond. This may reflect differences in vulnerability of larvae without lamellae between pond types. Such context-dependent responses in activity to kairomones should be kept in mind when evaluating the ability of a prey to recognize kairomones.     

Behavioural differences in starving herring Clupea harengus L. larvae correlate with body levels of essential fatty acids

Twenty days after hatching, a single stock of Atlantic herring ( Clupea harengus L.) larvae, cultured in the presence of rotifers and Artemia nauplii but showing little or no active feeding behaviour, displayed clear signs of starvation. Three groups of fish were distinguished: group I was generally pinhead-shaped, tended to swim with a spinning motion and floated vertically; group 2 lay moribund on the bottom of the tank; group 3 showed normal, active swimming behaviour. Fatty acids of total lipid extracted from groups 1 and 2 differed from group 3 in having markedly reduced percentages of 20:5n-3, 22:6n-3, 20:1 and 22:1. We conclude that individuals within a single stock of cultured herring larvae respond differently to starvation and that this generates well defined behavioural differences which correlate with levels of n-3 polyunsaturated fatty acids (PUFA) in body lipid. The implications of these observations are discussed.     

Contests between larval damselflies: empirical steps toward a better ESS model

Some hypotheses about facultatively aggressive interactions among damselfly larvae (Odonata: Zygoptera) have recently been generated from a model (Crowley 1984) based on the theory of evolutionarily stable strategies (ESS). The present study tests some of the assumptions and predictions of this ESS model with larvae of the damselfly Ischnura elegans van der Lind. in two sets of laboratory experiments. In contest experiments, interactions between two larvae on a thin dowel were observed in all possible combinations of the final three instars. The tendency to maintain control of the site and to evict the opponent was positively related to hunger, relative size (instar difference), and aggressiveness (labial striking), but negatively related to advancing toward a similar-sized opponent along the dowel. Contests were longer and involved more physical contact when larvae were more similar in size. No injuries or mortality resulted from the observed encounters. In distraction experiments, individual larvae were placed in a small feeding chamber with daphnid prey. Experimental larvae were surrounded by last-instar larvae visible through clear plastic walls; controls had no surrounding larvae. Time spent staring at others carried a feeding cost. This cost, the observed negative-exponential distributions of contest duration, and the apparent rarity of dangerous aggression, suggest that contests between similar-sized larvae could be considered wars of attrition. Other possible interpretations and some implications of these behaviour patterns for vulnerability to other predators are noted.     

Temperature,salinity tolerance,and buoyancy during early development and starvation of Clyde and North Sea herring,cod, and flounder larvae

Tolerance limits, at which 50% of larvae could survive high temperature and low salinity for 24 h, were determined for the yolk-sac larvae of Clyde and North Sea herring (Clupea harengus L.), cod (Gadus morhua L.) and flounder (Platichthys flesus L.) during early development and starvation. Clyde and North Sea herring, cod and flounder from hatching to the end of the yolk-sac stage, could withstand 21–23.5 °C, 20.5–23 °C, 15.5–18 °C and 21.5–24°C, respectively. The temperature tolerance was reduced by about 3.5–4 °C for Clyde herring and cod, 4–4.5 °C for North Sea herring and 8–8.5 °C for flounder when the larvae reached the point-of-no-return (PNR, when 50% of larvae, although still alive, are no longer strong enough to feed). The lowest salinity tolerance between hatching and the end of yolk-sac stage was 1–1.5‰ for Clyde and North Sea herring, 2–3‰ for cod and 0–1‰ for flounder. In no instance was there a loss of tolerance to low salinity during starvation. In fact, tolerance improved somewhat until the larvae became moribund. At hatching Clyde and North Sea herring larvae were negatively buoyant with a sinking rate of 0.35–0.4cm · s⁻¹ which steadily decreased until the larvae became moribund. Cod and flounder larvae, however, were positively buoyant at hatching but became progressively less buoyant and, by the end of the yolk-sac stage they were negatively buoyant with a sinking rate of 0.06–0.07 cm · s⁻¹. This sinking rate then decreased slightly until the PNR stage. The low salinity tolerance of all three species varied in a similar fashion to buoyancy.     

Size-dependent flight initiation by a lotic mayfly in response to a predatory fish

1. Laboratory experiments were performed to determine whether flight initiation by lotic mayfly larvae of Baetis tricaudatus exposed to the longnose dace ( Rhinichthys cataractae ) is affected by an individual's size and its physiological state.
2. We used a three factorial ANOVA design to test whether flight initiation distances (FIDs) were affected by Baetis size (small, large), starvation level (low, high), and the length of a predator-free foraging period (short, long).
3. FIDs were significantly affected by the interaction between Baetis size and starvation level, and the main level effects of starvation and Baetis size. FIDs of small larvae were unaffected by starvation level and the length of the predator-free feeding period, whereas starvation reduced FIDs of large larvae 2-fold.
4. Subsequent experiments showed that size-dependent differences in FIDs could not be attributed to size-specific differences in the economics of rates of food intake or gut evacuation. For both small and large larvae, food intake rates declined with increasing time spent foraging and both small and large larvae consumed the majority (70–75%) of food within the first 3 h of the 12-h feeding period. Similarly, gut evacuation declined with increasing starvation time and rates of evacuation did not differ between small and large larvae. These data suggest that size-dependent differences in flight initiation by Baetis larvae do not involve the energetics of food intake or processing.     

Influence of temperature on evasive responses of Atlantic herring larvae attacked by yearling herring, Clupea harengus L.

Predation encounters were staged in the laboratory between yearling herring, Clupea harengus L., 66 to 104 mm t.l. , and herring larvae, 8 to 30 mm t.l. ., at 8,11 and 14 o C. Video records were used to quantify prey behaviour. Prey responsiveness, reactive distance, response latency, and apparent looming threshold were not affected by temperature. Response speeds increased with temperature. Predator error rate and capture success showed no consistent thermal effects. Although the experiments could not fully evaluate the influence of temperature on the predators, results suggest that the predator's performance largely governs the outcome of an attack on a larva and that higher temperatures favour the predator by increasing the frequency of its encounter with prey.     

Size-dependent flight initiation by a lotic mayfly in response to a predatory fish

1. Laboratory experiments were performed to determine whether flight initiation by lotic mayfly larvae of Baetis tricaudatus exposed to the longnose dace ( Rhinichthys cataractae ) is affected by an individual's size and its physiological state.
2. We used a three factorial ANOVA design to test whether flight initiation distances (FIDs) were affected by Baetis size (small, large), starvation level (low, high), and the length of a predator-free foraging period (short, long).
3. FIDs were significantly affected by the interaction between Baetis size and starvation level, and the main level effects of starvation and Baetis size. FIDs of small larvae were unaffected by starvation level and the length of the predator-free feeding period, whereas starvation reduced FIDs of large larvae 2-fold.
4. Subsequent experiments showed that size-dependent differences in FIDs could not be attributed to size-specific differences in the economics of rates of food intake or gut evacuation. For both small and large larvae, food intake rates declined with increasing time spent foraging and both small and large larvae consumed the majority (70–75%) of food within the first 3 h of the 12-h feeding period. Similarly, gut evacuation declined with increasing starvation time and rates of evacuation did not differ between small and large larvae. These data suggest that size-dependent differences in flight initiation by Baetis larvae do not involve the energetics of food intake or processing.     

Vulnerability of late larval and early juvenile Atlantic herring, Clupea harengus, to predation by whiting,Merlangius merlangus

Laboratory experiments investigated changes in the vulnerability of herring to predation by whiting during growth from <34 to >80mm in length, Premetamorphic herring (<50mm) failed to react to c . 50% of attacks by the predator, but this was reduced to c . 20% in postmetamorphic fish. Premetamorphic herring failing to react had c. 30% probability of survival due to unforced errors by the predator (unsuccessful attacks that did not elicit a reaction by the prey), but these errors did not occur after herring metamorphosis. The loss of the advantage of lower conspicuousness following metamorphosis was counterbalanced by increased reactivity. Antipredator benefits should increase with schooling behaviour (first evident in experiments at c . 50 mm), so predation mortality should decrease in postmetamorphic herring in the sea. Metamorphosis itself would be associated with high predation risk since conspicuousness is enhanced but reactivity and schooling behaviour are still not fully developed.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

The influence of larval case design on vulnerability of Limnephilus frijole (Trichoptera) to predation

• 1 We examined the potential selective pressures exerted by different types of predators on morphological prey defences using the case-building larvae of the limnephilid caddisfly, Limnephilus frijole. The predators were a predaceous minnow, Gila pandora, and an aeschnid dragonfly naiad, Oplonaeschna armata.
• 2 The influence of larval case design on vulnerability to predators was evaluated in a series of laboratory experiments. Larval L. frijole were collected from a stream without fish or dragonflies. In the laboratory, larvae still occupying their field-built cases were exposed to the two predators, with which L. frijole co-occurs in other streams. Following 24 h exposure of caddisfly larvae to a specific predator, the pre-trial case length, case strength, case width, and case composition of victims and survivors were compared.
• 3 Principal components analysis (PCA) indicated substantial independent variation for all four case parameters in the study population. The cases of larvae surviving exposure to either dragonfly naiads or fish were significantly stronger and wider than cases of victims of predation. Cases of survivors were also longer and had a greater mineral fraction than those of victims, but differences were either marginally significant or not significant.
• 4 These results demonstrate that specific aspects of case design affect the vulnerability of caddisfly larvae. In addition, predaceous fish and predaceous invertebrates, using different predation techniques, may exert similar selective pressures on these defenses. Case aspects influencing vulnerability in these experiments are broadly consistent with natural variation in case design associated with predator-rich and predator-free habitats for related caddisfly species.

     

Effects of alternative prey on predation intensity from herring Clupea harengus and sandeel Ammodytes marinus on capelin Mallotus villosus larvae in the Barents Sea

Stomach contents from lesser sandeel Ammodytes marinus and herring Clupea harengus caught at one and three stations, respectively, were analysed to investigate predation intensity on capelin Mallotus villosus larvae. Most capelin larvae were found in the anterior sections of the stomachs close to the oesophagus, indicating that rapid digestion rates of larvae reduced the abundance in the posterior sections. The anterior sections of the stomachs had alternating layers of either copepods or capelin larvae and krill. This shows that the individual predators switched between feeding on either copepods or on krill and capelin larvae. A total of 549 capelin larvae was found in 440 fish stomachs. Capelin larvae were found in 20% of the sandeel stomachs, and 24, 34 and 62% of the stomachs from the three herring stations, respectively. Many of the predator stomachs contained more than five larvae, and up to 28 larvae were found in one herring stomach. The herring appeared to prey selectively on the largest capelin larvae, and the number of larvae per stomach was much higher in stomachs where krill had recently been eaten than where copepods were dominant. The predation intensity measured in this study is much higher than reported in earlier studies, and it is suggested that the predators were feeding using a searching image, and that the concentrations of alternative prey (copepods and krill) varied around a switching threshold.     

Ontogenetic- and condition-related effects of starvation on responsiveness in herring larvae (Clupea harengus L.) during repeated attacks by a model predator

The escape behaviour of fed and food-deprived herring larvae (20-30 mm SL) was studied during repeated attacks with a glass probe in order to investigate the causal mechanisms of starvation-induced changes in reaction to predators. Two experiments were set up: one where the fed and starved larvae were of the same age but of different sizes and one with groups of similar size but different ages. Biochemical and morphological condition measures described the condition of individual larvae. Starved larvae showed a lower responsiveness than fed larger larvae of the same age, and the responsiveness in this experiment decreased with decreasing nutritional status of the larvae. However, starved larvae that were of the same size but older than fed larvae showed a higher responsiveness, which could be explained by differences in development of sensory systems. A combination of condition and developmental factors thus explained the differences between starved and fed larvae. Both starved and fed larvae showed decreasing responsiveness over time with repeated attacks with no difference between starved and fed larvae in the relative change over time. The results emphasise the importance of taking into account individual age and/or development when the nutritional condition of wild-caught larvae is incorporated in survival models.     

Threat-sensitive Predator Avoidance by Larval Pacific Treefrogs (Amphibia, Hylidae)

According to the threat-sensitive predator avoidance hypothesis, the intensity of a prey animal's antipredator response should reflect its vulnerability to a specific predator. In laboratory experiments, we observed the intensity of antipredator responses of Pacific treefrog ( Hyla regilla ) tadpoles to stimuli from caged larval northwestern salamander ( Ambystoma gracile ) predators. We varied the sizes of the tadpoles relative to the salamanders in an attempt to create differences in vulnerability of tadpoles to the salamander predators. After documenting the response of the tadpoles to the caged predator, we tested the tadpole's vulnerability to the predator by releasing the tadpole with the predator. We observed that as the relative size of the tadpoles to the caged salamanders increased, the antipredator response of the tadpoles decreased. These changes in behaviour closely mirrored changes in actual vulnerability to the predator. Our results provide experimental support for the threat-sensitive predator avoidance hypothesis.     

Behavioural and life history responses to predation risk by common frog tadpoles exposed to two predators during ontogeny

The presence of predators can induce changes in both the morphology and behaviour of Anuran larvae, affecting both their size and developmental stage at metamorphosis and, consequently, the fitness of adult individuals. Tadpoles have been shown to be capable of finely tuning their defensive responses according to the actual risk perceived, which is expected to vary according to the prey-to-predator size ratio. In this study, we exposed common frog (Rana temporaria) tadpoles (Gosner stages 28–30), for a period of 2 weeks, to the non-lethal presence of dragonfly larvae (Anax imperator) and backswimmers (Notonecta glauca). In such a narrow window of time, we expected behavioural responses to be similar for both predators and exposure to predation risk to have negligible effects on tadpole development and weight. Overall, tadpoles increased hiding behaviour and were less active when predators were present in the experimental mesocosms, but behavioural responses were constrained to the early phase of the ontogeny and were no longer used when tadpoles reached a threshold size. Developmental rate slightly slowed down for predator treatments in comparison to controls, possibly as a consequence of energetic investment in unrecorded morphological defences. Although variation in laboratory conditions and protocols makes it hard to compare the results of different experiments, our results contribute to verify the consistency of behavioural responses in Anuran larvae.     

Movement and disappearance of mountain birch defoliators are influenced by the interactive effects of plant architecture and induced resistance

Abstract. 1. Changes in herbivore movement and feeding behaviour may determine the efficacy of induced plant resistance by affecting the location of damage within the foliage and by modifying the vulnerability of herbivores to predators. 2. Observations of larval feeding sites were used to test whether induced resistance increased the movement of free‐living Epirrita autumnata Borkh. (Lepidoptera, Geometridae) larvae feeding on mountain birch [Betula pubescens ssp. czerepanovii (Orlova) Hämet‐Ahti]. The amount of defoliation at different canopy parts was measured to test the associated changes in the spread of damage within the foliage. 3. The architectural complexity of trees was measured to test its association with the disappearance of larvae from their hosts. The underlying hypothesis was that the architectural traits of the host plant could affect disappearance by influencing the frequency of herbivores encountering predators. 4. Distance between the consecutive feeding positions, the number of leaves damaged, and consumption of long shoot leaves all increased in trees with induced resistance. 5. Disappearance of larvae depended on the architectural complexity of trees. The effect of complexity differed between defoliation treatments, and may depend on the activity and number of predators in relation to the canopy size. 6. Accordingly, this study suggested that the interactive effects of plant architecture, induced resistance, and herbivore behaviour can determine the performance of herbivores on their host plant.     

Experimental Evidence of Threat-Sensitive Collective Avoidance Responses in a Large Wild-Caught Herring School

Aggregation is commonly thought to improve animals'' security. Within aquatic ecosystems, group-living prey can learn about immediate threats using cues perceived directly from predators, or from collective behaviours, for example, by reacting to the escape behaviours of companions. Combining cues from different modalities may improve the accuracy of prey antipredatory decisions. In this study, we explored the sensory modalities that mediate collective antipredatory responses of herring (Clupea harengus) when in a large school (approximately 60 000 individuals). By conducting a simulated predator encounter experiment in a semi-controlled environment (a sea cage), we tested the hypothesis that the collective responses of herring are threat-sensitive. We investigated whether cues from potential threats obtained visually or from the perception of water displacement, used independently or in an additive way, affected the strength of the collective avoidance reactions. We modified the sensory nature of the simulated threat by exposing the herring to 4 predator models differing in shape and transparency. The collective vertical avoidance response was observed and quantified using active acoustics. The combination of sensory cues elicited the strongest avoidance reactions, suggesting that collective antipredator responses in herring are mediated by the sensory modalities involved during threat detection in an additive fashion. Thus, this study provides evidence for magnitude-graded threat responses in a large school of wild-caught herring which is consistent with the “threat-sensitive hypothesis”.