Escape Response Performance Research Articles

Kinematic performance declines as group size increases during escape responses in a schooling coral reef fish

IntroductionEscaping predation is essential for species survival, but prey must effectively match their response to the perceived threat imposed by a predator. For social animals, one mechanism to reduce risk of predation is living in larger group sizes, which dilutes each individual's risk of capture. When a predator attacks, individuals from a range of taxa (e.g., fishes, sharks, and amphibians) perform an escape response, to evade the attack.MethodsUsing the schooling coral reef damselfish Chromis viridis, we assess if there is an optimal group size that maximizes both individual escape response performance as well as group cohesion and coordination following a simulated predator attack, comparing schools composed of four, eight, and sixteen fish. The escape response was assessed through simulated predator attacks, measuring escape latency, kinematics (average turning rate, and distance covered), and group dynamics (school cohesion and coordination). The experiments were conducted with varying group sizes to analyze the impact on escape performance and group behavior.ResultsWe found that fish in various group sizes exhibited no difference in their reaction timing to a simulated predator attack (i.e., escape latency), but larger groups exhibited slower kinematics (i.e., lower average turning rate and shorter distance covered during the escape response), potentially because larger groups perceived the predator attack as less risky due to safety in numbers. Both school cohesion and coordination (as measured through alignment and nearest neighbor distance, respectively) declined in the 100 ms after the predator's attack. While there was no impact of group size on alignment, larger group sizes exhibited closer nearest neighbor distances at all times.DiscussionThe findings suggest that larger group sizes in schooling coral reef fish may lead to energy conservation by displaying less costly behavioral responses to predator threats. This potential energy saving could be attributed to a higher threshold of perceived threat required to trigger a rapid escape response in larger groups. The study emphasizes the intricate interplay between individual and collective behaviors in response to predation and sheds light on the nuanced dynamics of group living in the face of predation.

Evolvability under climate change: Bone development and shape plasticity are heritable and correspond with performance in Arctic charr (Salvelinus alpinus).

Environmental conditions can impact the development of phenotypes and in turn the performance of individuals. Climate change, therefore, provides a pressing need to extend our understanding of how temperature will influence phenotypic variation. To address this, we assessed the impact of increased temperatures on ecologically significant phenotypic traits in Arctic charr (Salvelinus alpinus). We raised Arctic charr at 5°C and 9°C to simulate a predicted climate change scenario and examined temperature-induced variation in ossification, bone metabolism, skeletal morphology, and escape response. Fish reared at 9°C exhibited less cartilage and bone development at the same developmental stage, but also higher bone metabolism in localized regions. The higher temperature treatment also resulted in significant differences in craniofacial morphology, changes in the degree of variation, and fewer vertebrae. Both temperature regime and vertebral number affected escape response performance, with higher temperature leading to decreased latency. These findings demonstrate that climate change has the potential to impact development through multiple routes with the potential for plasticity and the release of cryptic genetic variation to have strong impacts on function through ecological performance and survival.

Beyond black and white: divergent behaviour and performance in three rapidly evolving lizard species at White Sands

Determining which traits enable organisms to colonize and persist in new environments is key to understanding adaptation and ecological speciation. New environments can present novel selective pressures on colonists' morphology, behaviour, and performance, collectively referred to as ecomorphology. To investigate ecomorphological change during adaptation and incipient ecological speciation, we measured differences in morphology (body shape and size), behaviour (startle response), and performance (sprint speed) in three New Mexican lizard species: Holbrookia maculata, Sceloporus undulatus, and Aspidoscelis inornata. Each species is represented by dark morphs, cryptic on the brown adobe soils of the Chihuahuan Desert, and white morphs, cryptic on the gypsum substrate of White Sands. For each species, we then determined the effects of morphology and startle response on sprint speed on matched and mismatched substrate. For two of the three species, white morphs had larger body size and longer limbs. However, we found no statistical evidence that these morphological differences affected sprint speed. Colour morphs also exhibited different escape responses on the two substrates: in all species, dark morphs were less likely to immediately sprint from a simulated predator on white sand. As a result, escape response had a significant effect on sprint speed for two of the three species. Not surprisingly, all lizards sprinted faster on dark soil, which was probably due to the lizards' more immediate escape response and the higher compaction of dark soil. The relationship between escape response and sprint performance across the dark soil and white sand habitats suggests that behavioural differences may be an important component of adaptation and speciation in new environments. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 169–182.

Escape responses by jet propulsion in scallops

The impressive swimming escape response of scallops uses a simple locomotor system that facilitates analysis of the functional relationships between its primary components. One large adductor muscle, two valves, the muscular mantle, and the rubbery hinge ligament are the basic elements allowing swimming by jet propulsion. Although these basic functional elements are shared among scallop species, the exact nature of the escape response varies considerably within and among species. Valve shape and density have opposing influences upon the capacity for swimming and the ease of attack by predators once captured. Patterns of muscle use can partly overcome the constraints imposed by shell characteristics. The depletion of muscle reserves during gametogenesis leads to a trade-off between escape response performance and reproductive investment. However, changes in muscle energetic status influence repeat performance more than initial escape performance. Escape response performance is influenced by habitat temperature and mariculture techniques. During scallop ontogeny, changes in susceptibility to predation and in reproductive investment may influence escape response capacities. These ontogenetic patterns are likely to vary with the longevity and maximal size of each species. Although the basic elements allowing swimming by jet propulsion are common to scallops, their exact use varies considerably among species.

Repeatability of escape response performance in the queen scallop (Aequipecten opercularis)

In order for natural selection to operate, physiological and behavioural traits must exhibit both inter-individual variability and intra-individual consistency (i.e. repeatability) in performance. In this study, we describe individual variation and temporal repeatability in the escape responses of the queen scallop, Aequipecten opercularis, and determine whether individuals exhibited consistently high or low rankings in different aspects of the escape response. Five measures of individual performance were recorded on four occasions (days 0, 2, 7 and 28), providing proxies for sensory acuity (response latency), immediate and sustained swimming performance (burst and average clap rates), and swimming endurance (total number of claps and total time spent clapping). All components of the escape response exhibited significant inter-individual variability (all P<0.0001). Escape response latency, burst clap rate, total number of claps and total duration spent clapping maintained significant repeatability over 28 days (all P<0.016). Average clap rate was repeatable in the short term (2 days, P<0.0001) but repeatability declined by 28 days (P=0.097). Concordance analysis indicated that individuals maintained the same performance rankings over time for each component of the escape response (all P<0.001). In addition, some individuals ranked as consistently high or low performers across response latency, burst and average clap rate, and total number of claps. An individual's ability to evade predators through the provision of an escape response of an appropriate magnitude, subject to physiological, behavioural and organismal constraints, will have clear fitness-related consequences.

Fatty acid content of eggs determines antipredator performance of fish larvae

Recent work has suggested that provisioning of eggs with certain critical nutrients could be a more meaningful measure of maternal investment and correlate of offspring fitness than traditional measures of egg size. The aim of our study was to assess variability in egg quality and larva quality and to identify connections between them and the implications for larval survival. Egg size, proximate composition, and fatty acid composition were measured for 40 batches of eggs from 8 captive pairs of red drum (Osteichthyes: Sciaenops ocellatus). We reared larvae from these batches of eggs to a common size (10mm total length, 2–3weeks posthatching) and assessed routine activity and escape response performance of 671 individuals. Egg fatty acid composition varied more than egg size or proximate composition. Concentrations of certain long chain, highly unsaturated essential fatty acids (e.g., arachidonic acid and docosahexaenoic acid) were the only egg traits that were significantly related to larva quality (measured as escape performance). Reduced escape performance of larvae from eggs with low fatty acid concentrations was not compensated by 3weeks of feeding on a diet enriched with fatty acids, suggesting irreversible developmental effects. Since fatty acids in eggs originate from the maternal diet, offspring survival may be determined in part by availability of nutrient-rich prey to pre-spawning adults. Migrations, regime shifts, and exploitation of marine communities could operate through this mechanism to influence recruitment in fish populations. Our findings underscore the importance of non-genetic maternal contributions to egg quality and the linkage between environmental conditions experienced by adult females and offspring fitness.

Diet and performance in the scallop,Argopecten purpuratus: force production during escape responses and mitochondrial oxidative capacities

We examined whether escape response performance and mitochondrial capacities could reveal differences created by feeding scallops, Argopecten purpuratus, mono-specific algal diets composed of either Chaetoceros calcitrans or Isochrysis galbana (variety T. iso) hereafter T. iso. Before and after feeding scallops with these diets, we assessed force production in vivo to evaluate escape response performance (initial and repeat). We measured oxidative capacities of mitochondria isolated from the adductor muscle and from the male and female portions of the gonad. Initial escape response performance was reduced more by the C. calcitrans diet than by the T. iso diet. Repeat escape responses, which require aerobic recuperation, were reduced by both treatments. The oxidative capacity of mitochondria isolated from muscle and female gonad was markedly lower in scallops fed C. calcitrans than in those fed T. iso. Flux through complex I–IV and through complex IV was also lower in mitochondria from muscle of scallops fed C. calcitrans than in those fed T. iso. Muscle aerobic capacity, assessed by citrate synthase activity, was lower in scallops fed C. calcitrans than in those fed T. iso. Despite the marked differences in fatty acid (FA) composition of the algal diets, the FA composition of mitochondrial phospholipids differed little between scallops fed C. calcitrans and those fed T. iso. Both escape response behaviour and mitochondrial capacities changed with feeding mono-specific diets. The simplicity of measurements of scallop escape responses suggests this as a practical means of evaluating the status of scallops for the two monoalgal diets tested.

Allozyme heterozygosity and escape response performance of the scallops, Argopecten purpuratus and Placopecten magellanicus

Multilocus allozyme heterozygosity (MLH) has been positively correlated with growth in some marine bivalves and was suggested to facilitate swimming activity in pectinids. Using two highly mobile scallops, Placopecten magellanicus and Argopecten purpuratus, we examined escape response performance and morphometric characteristics as a function of allelic variability at metabolic loci. Ten allozyme systems were used for A. purpuratus and 7 for P. magellanicus. In each species, the morphometric characteristics and escape response parameters were analyzed separately using principal components analysis (PCA) and the scores of the major principal components were related to allozyme heterozygosity. In both P. magellanicus and A. purpuratus, positive correlations were found between MLH and morphometric parameters, but escape response parameters were only positively linked to MLH in P. magellanicus, and then weakly. The hypothesis that MLH improves fitness of pectinids by increasing the capacity to escape predators is not supported.

Thermal sensitivity of escape response performance by the scallop Placopecten magellanicus: Impact of environmental history

To examine the impact of environmental history on the thermal sensitivity of escape response performance in juvenile giant scallops, Placopecten magellanicus, we compared animals sampled in late May, when water temperatures and day length were increasing, to animals sampled in late September, when water temperature and day length were decreasing. Habitat temperature was approximately 12 °C at both sampling times. For May scallops, performance was better at 6 than at 12 or 18 °C whereas September scallops performed better at 6 and 12 °C than at 19 °C. Regardless of environmental history, the rate of phasic contractions consistently declined at 18–19 °C, due to a decrease in the number of phasic contractions. Force measurements during escape responses of May scallops showed that phasic force production and the minimal interval between contractions changed little with temperature, whereas the minimum and mean durations of phasic contractions decreased as temperature rose. Phasic contraction rate in the first series increased with temperature. Reliance upon tonic contractions was higher in scallops tested at 18 °C than in those tested at 6 °C. Environmental history, more than habitat temperature at the time of sampling, seems to set the thermal sensitivity of phasic contraction rate in P. magellanicus. Phasic force production did not change within the thermal range tested.

Locomotion versus spawning: escape responses during and after spawning in the scallop Argopecten purpuratus

The energetic cost of spawning and the endogenous factors that modulate spawning could modify escape response performance, leading to a conflict between the requirements of two fundamental components of fitness: reproduction and survival. We examined whether spawning changed force production during escape responses by the functionally hermaphroditic scallop, Argopecten purpuratus, and whether the response of smooth (tonic) and striated (phasic) muscles differed. Force production during escape responses by mature scallops was compared before induction of spawning, during spawning and after completion of spawning. Maximum tonic force and the area under the force curve (total force recorded) were diminished during gamete release, whereas phasic force production (maximum and mean force) increased after spawning was completed. The number and frequency of phasic contractions did not change during the spawning process, suggesting that spawning did not limit fuel availability for phasic contractions. The decrease in tonic force during spawning and the increased phasic force production after spawning may reflect changes in monoamine levels during gamete release. Whereas the spawning process modified force production during escape responses, the changes would, if anything, enhance escape performance during an initial encounter between a scallop and a predatory sea star.

Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus

In scallops, gametogenesis and spawning can diminish the metabolic capacities of the adductor muscle and reduce escape response performance. To evaluate potential mechanisms underlying this compromise between reproductive investment and escape response, we examined the impact of reproductive stage (pre-spawned, spawned and reproductive quiescent) of the giant scallop, Placopecten magellanicus, on behavioural (i.e., escape responses), physiological (i.e., standard metabolic rates and metabolic rates after complete fatigue) and mitochondrial capacities (i.e., oxidative rates) and composition. Escape responses changed markedly with reproductive investment, with spawned scallops making fewer claps and having shorter responses than pre-spawned or reproductive-quiescent animals. After recuperation, spawned scallops also recovered a lower proportion of their initial escape response. Scallop metabolic rate after complete fatigue (VO2max) did not vary significantly with reproductive stage whereas standard metabolic rate (VO2min) was higher in spawned scallops. Thus spawned scallops had the highest maintenance requirements (VO2min/VO2max). Maximal capacities for glutamate oxidation by muscle mitochondria did not change with reproductive stage although levels of ANT and cytochromes as well as cytochrome C oxidase (CCO) activity did. Total mitochondrial phospholipids, sterols and the proportion of phospholipid classes differed only slightly between reproductive stages. Few modifications were detected in the fatty acid (FA) composition of the phospholipid classes except in cardiolipin (CL). In this class, pre-spawned and spawned scallops had fairly high proportions of 20:5n-3 whereas this FA in reproductive-quiescent scallops was threefold lower and 22:6n-3 was significantly higher. These changes paralleled the increases in CCO activity and suggest an important role of CL on the modifications of CCO activity in scallops. However, mitochondrial properties could not explain the decreased recuperation ability from exhausting exercise in spawned scallops. Shifts in maintenance requirements (VO2min/VO2max) and aerobic scope (VO2max − VO2min) provided the best explanation for the impact of reproduction on escape response performance.

Force recordings during escape responses by Placopecten magellanicus (Gmelin ): Seasonal changes in the impact of handling stress

Handling stress coupled with air exposure reduced the contractile performance during escape responses of 2+ scallops, Placopecten magellanicus, modifying maximal and mean phasic force production, the number of phasic contractions and the minimal interval between phasic contractions as well as reducing maximal tonic force production and increasing the reliance upon tonic contractions. The impact of handling stress was mitigated in scallops studied in the fall (late October) relative to the summer (late June and late August), with smaller declines in performance for all parameters examined. Seasonal changes in escape response performance by unstressed scallops were few, with virtually no change in maximal or mean phasic force production, in the number of phasic contractions or in the minimal interval between phasic contractions. As the scallops sampled in October had lower condition indices than those sampled in summer, the reduced impact of handling stress was likely due to the lower air and water temperatures. This suggests that transfers of juvenile scallops during culture operations should be done during cooler periods. Force measurements during escape responses are a sensitive, but simple tool with which to assess the status of scallops as they clearly reveal the marked impact of handling stress as well as more subtle seasonal changes.

The escape response of food-deprived cod larvae ( Gadus morhua L.)

The escape response of Atlantic cod larvae ( Gadus morhua) 25 and 47 days post hatch (dph) – either fed or deprived of food for three days – was studied. Larval escape responses were provoked by water movement from the suction of a fixed-position pipette. Escape latency, distance, speed, burst speed, and vertical and lateral escape angles were quantified using motion tracking software designed for 3-D silhouette video recordings. Escape performance, expressed as escape distance and escape speed, improved with age. The escape angles were normally distributed and highly variable, ranging from − 170° to 170° and − 40° to 105° for lateral and vertical escape angles respectively. No food deprivation-induced effects in any of the behaviours were found, suggesting that there are no condition-related behavioural effects (size-independent effects) in escape response performance after 3 d of food deprivation. This may reflect a negligible difference in the cost/benefit equation for fed vs. food-deprived larvae in performing an escape response when under attack.

Swimming Performance, Metabolic Rates, and Their Correlates in the Iceland ScallopChlamys islandica

The dramatic escape response of some scallops is modified by reproductive investment and by acclimation temperature. Despite considerable knowledge of the physiology of the escape response, functional links between escape response performance, organismal rates of oxygen uptake, and tissue metabolic capacities are little known. We measured oxygen consumption rates (standard, maximal, and aerobic scope), escape behavior (initial and repeat performance), tissue mass, condition index, protein content, and tissue metabolic capacities in the Iceland scallop Chlamys islandica to examine links between these parameters. Postexercise oxygen consumption rates were positively linked to contraction rate (repeat test) and to pyruvate kinase activity in the adductor muscle but negatively linked to digestive gland wet mass. Swimming behavior was mainly related to activity of glycolytic enzymes, and enzymatic activities were related to anatomic parameters. Scallop behavior and physiology change with size, both within our samples and on a larger scale. Small scallops showed more intense swimming activity and had higher arginine kinase activities but lower glycolytic enzyme activities in their adductor muscle than larger scallops. This corresponds to the ontogenetic change in susceptibility to predation and in habitat use observed in C. islandica.

Development of the Escape Response in Teleost Fishes: Do Ontogenetic Changes Enable Improved Performance?

Teleost fishes typically first encounter the environment as free-swimming embryos or larvae. Larvae are morphologically distinct from adults, and major anatomical structures are unformed. Thus, larvae undergo a series of dramatic morphological changes until they reach adult morphology (but are reproductively immature) and are considered juveniles. Free-swimming embryos and larvae are able to perform a C-start, an effective escape response that is used evade predators. However, escape response performance improves during early development: as young fish grow, they swim faster (length-specific maximum velocity increases) and perform the escape more rapidly (time to complete the behavior decreases). These improvements cease when fish become juveniles, although absolute swimming velocity (m s(-1)) continues to increase. We use studies of escape behavior and ontogeny in California halibut (Paralichthys californicus), rainbow trout (Oncorhynchus mykiss), and razorback suckers (Xyrauchen texanus) to test the hypothesis that specific morphological changes improve escape performance. We suggest that formation of the caudal fin improves energy transfer to the water and therefore increases thrust production and swimming velocity. In addition, changes to the axial skeleton during the larval period produce increased axial stiffness, which in turn allows the production of a more rapid and effective escape response. Because escape performance improves as adult morphology develops, fish that enter the environment in an advanced stage of development (i.e., those with direct development) should have a greater ability to evade predators than do fish that enter the environment at an early stage of development (i.e., those with indirect development).

A comparison of startle response in two morphs of the brook stickleback (Culaea inconstans): Further evidence for a trade-off between defensive morphology and swimming ability

It is generally thought that predation pressure drives the evolution of long spines and robust pelvic girdles in sticklebacks (Pisces: Gasterosteidae). However, the lack of these traits in some environments with intense predation pressure suggests that there may be a limit to which apparently defensive structures benefit sticklebacks. This paper focuses on a trade-off between defensive morphology and escape response performance in a genetically based polymorphic population of brook stickleback (Culaea inconstans), in which fish have fully developed pelvic girdles and pelvic spines (‘complete’ morph) or completely lack these defensive structures (‘absent’ morph). Startle response experiments revealed that the absent morph did better in all aspects of startle performance (displacement, maximum velocity, acceleration) than the complete morph. The absent morph also bent deeper than the complete morph during the initial phase of the startle response. The pelvic girdle polymorphism in this population may be maintained because individuals with a complete pelvic girdle and spines may be able to escape more easily from predators once they are captured, whereas individuals lacking these structures may better avoid capture when they are attacked.

Developmental changes in escape response performance of five species of marine larval fish

We measured the escape response performance by four species of larval fish: Atlantic cod (Gadus morhua), Atlantic herring (Clupea harengus harengus), radiated shanny (Ulvaria subbifurcata), and capelin (Mallotus villosus). The resultant data were combined with information from larval winter flounder (Pleuronectes americanus) to produce general models relating escape response performance to larval size. Three components of the escape response produced models with reasonable predictive ability, including mean and maximum speed during the response, and the distance travelled by larvae during the first 100 ms of the response (the latter representing the contribution of the C-shaped fast start that initiates the response). The logarithm of mean and maximum escape speed increased linearly with increasing larval length. The distance after 100 ms was linearly related to larval length. Our general model for mean escape speed produced significantly higher length-specific speed values than did the general model proposed by Miller et al. (T.J. Miller, L.B. Crowder, J.A. Rice, and E.A. Marschall. 1988. Can. J. Fish. Aquat. Sci. 45: 1657n1670). Resume : Nous avons mesurO liefficacitO de la rOaction de fuite chez les larves de quatre poissons : la morue (Gadus morhua), le hareng (Clupea harengus harengus), liulvaire deux-lignes (Ulvaria subbifurcata) et le capelan (Mallotus

Developmental changes in escape response performance of five species of marine larval fish

Developmental changes in escape response performance of five species of marine larval fish

Evidence for a trade-off between defensive morphology and startle-response performance in the brook stickleback (Culaea inconstans)

It is generally believed that predation pressure may drive the evolution of long spines, a robust pelvic girdle, and a deep body in sticklebacks (Pisces: Gasterosteidae). However, the lack of such traits in environments under intense predation pressure suggests that there may be a limit to which these apparently defensive structures benefit sticklebacks. In some environments, well-developed defensive structures may not increase stickleback survival, but may actually reduce fitness if there is a cost associated with them. This paper focuses on a trade-off between defensive morphology and escape-response performance in the brook stickleback (Culaea inconstans). Our study of four populations of brook stickleback reveals that the population with the largest pelvic girdles and deepest bodies has a poorly developed escape response (i.e., small displacement, low maximum velocity, and low acceleration), while the population with the smallest pelvic girdles and shallowest bodies has a highly developed escape response. The two populations with intermediate defensive structures are intermediate in escape-response performance. Consideration of predation regimes in different environments may help us understand selection pressures that favor heavily versus poorly armored stickleback morphs.