Swimming in the sea hare Aplysia brasiliana: Cost of transport, parapodial morphometry, and swimming behavior

The energetics and behavior of the parapodial-swimming Aplysia brasiliana were investigated in order to compare net cost of transport (COT_net) between swimming and crawling, and to compare transport costs with other swimmers. Oxygen consumption (V_O2) increased with increasing animal mass for resting, crawling, and swimming animals. Slopes of the regressions of log V_O2 on log mass were 0.90, 0.91, and 0.89 for resting, crawling, and swimming, respectively. The regression for resting V_O2 on mass was significantly lower than regressions of crawling and swimming on mass, which fell into a statistically homogenous subgroup. During 4-h swimming bouts, parapodial beat frequency dropped by less than 10% of starting values after 2 h and then stabilized for the remainder of the trial, whereas velocity steadily decreased to about 70% of starting values over the 4-h period. Initial beat frequency (at the start of a swimming bout) was negatively related to body mass, varying from 1.1 beat s^− 1 for a 34 g individual to 0.7 beats s^− 1 for a 500 g individual. Final beat frequency (at the end of a swimming bout) was also negatively related to body mass, but had a significantly lower intercept than initial beat frequency. Neither initial swimming velocity nor final swimming velocity was related to mass, but final velocity was significantly lower than initial velocity. A 250 g A. brasiliana swam at 345 m h^− 1 and crawled at 7 m h^− 1. Swimming COT_net (0.1 ml O₂ kg^− 1 m^− 1) for a 250 g A. brasiliana was 50 times less than crawling COT_net (5.3 ml O₂ kg^− 1 m^− 1). While the crawling COT_net for A. brasiliana fell within the range of other marine gastropods, swimming COT_net was less than that of swimming crustaceans, and much less than another gastropod, Melibe leonina, that uses lateral bending to swim.     

Responses of the sea catfish Ariopsis felis to chemical defenses from the sea hare Aplysia californica

Ink secretion of sea hares (Aplysia spp.), which is a mixture of co-released ink from the ink gland and opaline from the opaline gland, protects sea hares from predatory invertebrates through diverse mechanisms. These include both aversive or deterrent compounds and also high concentrations of amino acids that stimulate the predators' chemical senses and divert the attack through phagomimicry or sensory disruption. The aim of the present study was to examine if sea hares also defend themselves from predatory vertebrates by interacting with their chemical senses. We used sea catfish, Ariopsis felis, in behavioral and electrophysiological experiments. Behavioral tests on sea catfish show that ink is aversive: when ink is added to palatable food items (noodles with food flavoring), the noodles are no longer eaten, and when ink is added to noodles without food flavoring, the noodles are avoided more than unflavored noodles. Behavioral tests also show that opaline and the amino acid components of either opaline or ink are appetitive. Electrophysiological recordings of chemosensory neuronal activity in the olfactory epithelium and maxillary barbels show that the olfactory and gustatory systems of sea catfish are highly stimulated by ink and opaline, and that the amino acid components of ink and opaline significantly contribute to these responses. Compounds generated by the activity of escapin, an L-amino acid oxidase in the secretion, are moderately stimulatory to both olfactory and gustatory systems. Taken together, our results support the idea that sea hares are chemically defended from predatory sea catfish largely through unpalatable chemical deterrents in ink, but possibly also through amino acids stimulating olfactory and gustatory systems and thus functioning through phagomimicry or sensory disruption.     

Acidity enhances the effectiveness of active chemical defensive secretions of sea hares, <Emphasis Type="Italic">Aplysia californica</Emphasis>, against spiny lobsters, <Emphasis Type="Italic">Panulirus interruptus</Emphasis>

Sea hares such as Aplysia californica, gastropod molluscs lacking a protective shell, can release a purple cloud of chemicals when vigorously attacked by predators. This active chemical defense is composed of two glandular secretions, ink and opaline, both of which contain an array of compounds. This secretion defends sea hares against predators such as California spiny lobsters Panulirus interruptus via multiple mechanisms, one of which is phagomimicry, in which secretions containing feeding chemicals attract and distract predators toward the secretion and away from the sea hare. We show here that ink and opaline are highly acidic, both having a pH of ∼5. We examined if the acidity of ink and opaline affects their phagomimetic properties. We tested behavioral and electrophysiological responses of chemoreceptor neurons in the olfactory and gustatory organs of P. interruptus, to ink and opaline of A. californica within their natural range of pH values, from ∼5 to 8. Both behavioral and electrophysiological responses to ink and opaline were enhanced at low pH, and low pH alone accounted for most of this effect. Our data suggest that acidity enhances the phagomimetic chemical defense of sea hares.     

Multiple components in ink of the sea hare Aplysia californica are aversive to the sea anemone Anthopleura sola

Sea hares of the genus Aplysia rely on an array of behavioral and chemical defenses, including the release of ink and opaline, to protect themselves from predation. While many studies have demonstrated that ink and opaline are repellent to predators, very little is known about which components of these secretions are active against predators. Ink was previously shown to facilitate the escape of Aplysia from predatory anemones (Anthopleura) by eliciting tentacle retraction and/or shriveling, and gastrovascular eversion, but the metabolites mediating this interaction were not identified. We investigated the metabolites in Aplysia californica secretions that were aversive to the anemone Anthopleura sola, as demonstrated by tentacle shriveling and/or retraction. We found that ink elicited tentacle shriveling and/or retraction, while opaline elicited a feeding response. The active components in ink do not appear to be diet-dependent, as ink was aversive regardless of diet (natural seaweed diet vs. Gracilaria ferox). Furthermore, metabolites extracted from G. ferox were not aversive, suggesting that the aversive components are produced by the sea hares. We then examined escapin, a protein in ink with antimicrobial properties. Escapin quickly forms reaction products when mixed with the amino acids l-lysine and l-arginine, which would occur when ink and opaline are released into the sea hare mantle cavity. Neither escapin alone nor escapin mixed with its amino acid substrate l-lysine elicited aversive behaviors either immediately before or 2 min before applying to the tentacles. In addition, escapin mixed with opaline and applied to tentacles after 2 min did not elicit a significant aversive response. Using bioassay-guided fractionation, we attempted to isolate the components in A. californica ink that are aversive to A. sola. We determined that multiple components in ink, including both lipophilic and hydrophilic constituents, elicited aversive responses. We hypothesize that these components may facilitate A. californica's escape from A. sola by eliciting tentacle shriveling and/or retraction, which lead to anemones dropping ensnared sea hares.     

Vulnerability of sea hares to fish predators: importance of diet and fish species

Many sea hares (Opisthobranchia, Anaspidea) sequester secondary metabolites from their algal diets. Tests of the hypothesis that sequestered metabolites deter predators have yielded ambiguous results. We manipulated secondary metabolites in vivo by collecting the sea hare Stylocheilus striatus from different host algae, and by raising it in the laboratory on artificial diets containing or lacking secondary metabolites (malyngamides A and B). Sea hares were then offered to fish. Fish identity affected vulnerability of sea hares to predation far more than did diet history. Wrasses and bream ate most sea hares tasted; damselfishes, goatfishes, and other fishes rejected most. Diet history affected vulnerability of sea hares to wrasses in one of four experiments, and if data from all experiments were pooled, but the effect was modest. Diet history did not affect vulnerability of sea hares to other fish taxa. Despite several studies, evidence for diet-derived defenses against predators in sea hares remains equivocal.     

The Quantitative Genetic Architecture of the Bold-Shy Continuum in Zebrafish,Danio rerio

In studies of consistent individual differences (personality) along the bold-shy continuum, a pattern of behavioral correlations frequently emerges: individuals towards the bold end of the continuum are more likely to utilize risky habitat, approach potential predators, and feed under risky conditions. Here, we address the hypothesis that observed phenotypic correlations among component behaviors of the bold-shy continuum are a result of underlying genetic correlations (quantitative genetic architecture). We used a replicated three-generation pedigree of zebrafish (Danio rerio) to study three putative components of the bold-shy continuum: horizontal position, swim level, and feeding latency. We detected significant narrow-sense heritabilities as well as significant genetic and phenotypic correlations among all three behaviors, such that fish selected for swimming at the front of the tank swam closer to the observer, swam higher in the water column, and fed more quickly than fish selected for swimming at the back of the tank. Further, the lines varied in their initial open field behavior (swim level and activity level). The quantitative genetic architecture of the bold-shy continuum indicates that the multivariate behavioral phenotype characteristic of a “bold” personality type may be a result of correlated evolution via underlying genetic correlations.     

Consequences of long-distance swimming and travel over deep-water pack ice for a female polar bear during a year of extreme sea ice retreat

Polar bears (Ursus maritimus) prefer to live on Arctic sea ice but may swim between ice floes or between sea ice and land. Although anecdotal observations suggest that polar bears are capable of swimming long distances, no data have been available to describe in detail long distance swimming events or the physiological and reproductive consequences of such behavior. Between an initial capture in late August and a recapture in late October 2008, a radio-collared adult female polar bear in the Beaufort Sea made a continuous swim of 687 km over 9 days and then intermittently swam and walked on the sea ice surface an additional 1,800 km. Measures of movement rate, hourly activity, and subcutaneous and external temperature revealed distinct profiles of swimming and walking. Between captures, this polar bear lost 22% of her body mass and her yearling cub. The extraordinary long distance swimming ability of polar bears, which we confirm here, may help them cope with reduced Arctic sea ice. Our observation, however, indicates that long distance swimming in Arctic waters, and travel over deep water pack ice, may result in high energetic costs and compromise reproductive fitness.     

North Sea ecosystem change from swimming crabs to seagulls

A recent increase in sea temperature has established a new ecosystem dynamic regime in the North Sea. Climate-induced changes in decapods have played an important role. Here, we reveal a coincident increase in the abundance of swimming crabs and lesser black-backed gull colonies in the North Sea, both in time and in space. Swimming crabs are an important food source for lesser black-backed gulls during the breeding season. Inhabiting the land, but feeding mainly at sea, lesser black-backed gulls provide a link between marine and terrestrial ecosystems, since the bottom-up influence of allochthonous nutrient input from seabirds to coastal soils can structure the terrestrial food web. We, therefore, suggest that climate-driven changes in trophic interactions in the marine food web may also have ensuing ramifications for the coastal ecology of the North Sea.     

A quantitative description of the behaviour of wild juvenile plaice (Pleuronectes platessa L.)

The behaviour of young plaice (Pleuronectes platessa L.) as they migrate up and down sandy beaches with the tide is described. Their behaviour during this migration consists mainly of swimming and feeding interspersed with rarer behavioural acts. Over short periods swimming behaviour can be described by a random model in which the probability of a swim occurring remains constant. This probability varies markedly, however, from hour to hour. Two types of swimming movement are recognized: one of very short duration represents searching for food and the other, longer, category serves to transport the fish up and down the shore. Variations in the feeding rate and in the frequency, duration, and direction of swimming movements over the tidal cycle are described and related to the changing physical and biological conditions that the fish experience during their intertidal movements.     

Comparison of vertical and horizontal swimming behaviour of the weather loach Misgurnus anguillicaudatus

Experiments on the swimming kinetics and behaviour of weather loach Misgurnus anguillicaudatus showed that horizontal swim speed was significantly greater than swim speeds when ascending to or descending from the water surface to gulp air. Vertical swimming speeds during ascending or descending were similar. Misgurnus anguillicaudatus swam unsteadily during vertical movements compared with horizontal movements.     

Interspecific variation in chemical defenses in the sea hares (Opisthobranchia: Anaspidea)

Most species of sea hares (Opisthobranchia: Anaspidea) sequester secondary metabolites from their algal diets in their digestive glands. Aplysia Juliana Quoy and Gaimard, 1832, a sea hare that feeds on Ulva spp. and Enteromorpha spp., algae with few or no secondary metabolites, were compared with the sympatric sea hares A. oculifera Adams and Reeve, 1850, A. kurodai (Baba, 1937), and Dolabella auricularia (Solander, 1786), all of which eat chemically rich algae, to see if sequestered secondary metabolites afford protection to sea hares from potential predators. Organic extracts of whole A. Juliana stimulated, and organic extracts of whole D. auricularia deterred feeding by crabs. However, tests with organic extracts of individual body parts indicated that this pattern was due almost exclusively to unpalatability of extracts of D. auricularia digestive glands. Tests with pieces of tissue from the exterior of the animals, or with extracts of such tissues, showed no consistent patterns indicating that A. Juliana were more palatable than other sea hares. Sea hare egg masses do not appear to contain diet-derived secondary metabolites. However, pieces of egg masses of A. Juliana and D. auricularia were universally rejected by crabs and reef fish, and extracts of A. Juliana egg masses deterred feeding by some reef fish. Finally, both opaline secretion of A. Juliana and ink of A. kurodai, but not ink of D. auricularia, none of which appear to contain diet-derived secondary metabolites, deterred feeding by crabs. Opaline secretion from A. Juliana, but not ink from A. kurodai, induced avoidance behavior in crabs. Although sequestered secondary metabolites clearly can affect the palatability of the digestive gland, there is little evidence that they affect the palatibility of the ink, opaline secretion, eggs, or skin, suggesting that sequestered secondary metabolites may not play a key role in anti-predator defense of sea hares.     

Escape by inking and secreting: marine molluscs avoid predators through a rich array of chemicals and mechanisms

Inking by marine molluscs such as sea hares, cuttlefish, squid, and octopuses is a striking behavior that is ideal for neuroecological explorations. While inking is generally thought to be used in active defense against predators, experimental evidence for this view is either scant or lacks mechanistic explanations. Does ink act through the visual or chemical modality? If inking is a chemical defense, how does it function and how does it affect the chemosensory systems of predators? Does it facilitate escape not only by acting directly on predators but also by being an alarm signal for conspecifics? This review examines these issues, within a broader context of passive and active chemical defensive secretions. It focuses on recent work on mechanisms of defense by inking in sea hares (Aplysia) and extends what we have learned about sea hares to other molluscs including the cephalopods.     

Behaviour of pelagic larvae of four coral-reef fish species in the ocean and an atoll lagoon

In-situ behaviour of settlement-stage larvae (10-30 mm) of four coral-reef fishes - Acanthurus triostegus, Chromis viridis, Neoniphon argenteus and Ptereleotris sp. - differed between lagoon and ocean at Rangiroa Atoll, Tuamotu Islands, French Polynesia. Divers released 130 larvae individually in midwater, and recorded larval swimming speed, depth and direction. All species swam faster than average currents, and C. viridis swam faster in the lagoon than in the ocean. Vertical distribution behaviour of all species differed between ocean and lagoon, generally by larvae swimming deeper in the ocean. Nearly all individual larvae swam directionally. Within a species, distribution of average bearings of individual larvae was not directional, nor did it differ between ocean and lagoon. Larvae detected predators 3-6 m away, and stopped or changed depth or direction to avoid them. We therefore reject the 'simplifying assumptions' that reef-fish larvae are passive or that their behaviour is independent of location. Behavioural flexibility of settlement-stage reef-fish larvae has implications for dispersal, retention and population connectivity. This constitutes the first report of larval reef-fish behaviour in the open ocean. However, in the ocean, many larvae descended rapidly below safe diving depth, and adult remoras interfered, making in-situ study of larval behaviour difficult.     

Charismatic microfauna alter cyanobacterial production through a trophic cascade

The trophic ecology of cyanobacterial blooms is poorly understood on coral reefs. Blooms of toxic cyanobacteria, Lyngbya majuscula, can quickly form large mats. The herbivorous sea hare, Stylocheilus striatus, and the predatory nudibranch, Gymnodoris ceylonica, often associate with these blooms, forming a linear food chain: nudibranch—sea hare—cyanobacteria. Using laboratory studies, this study quantified (1) the functional response of nudibranchs, (2) the effect of sea hare size on predation rates, and (3) the strength of the indirect effect of sea hare predation on cyanobacteria (i.e., a trophic cascade). Nudibranchs consumed on average 2.4 sea hares d^?1, with the consumption of small sea hares 22 times greater than the consumption of large sea hares. Predation of sea hares reduced herbivory. Cyanobacterial biomass was 1.5 times greater when nudibranchs were present relative to when nudibranchs were absent. Although sea hare grazing can substantially reduce cyanobacterial biomass, predation of sea hares may mitigate grazing pressure, and therefore increase the abundance of cyanobacteria.     

Anisotropy and shift of search behavior in Malabar grouper (<Emphasis Type="Italic">Epinephelus malabaricus</Emphasis>) larvae in response to prey availability

In order to enhance encounters with prey, planktonic predators may display different swimming behavior with respect to food availability and distribution. In this study, we used 3D video techniques to record the swimming behavior of malabar grouper (Epinephelus malabaricus) larvae in both the absence and the presence of prey (Artemia sp. nauplii). Swimming properties were investigated in all of the 3D, the two vertical, and the horizontal projections using scale-dependent (mean speed and Net to Gross Displacement Ratio) and scale-independent (fractal dimension) metrics. When prey was added, larvae swam slower and in a less convoluted way as compared to what was observed in the absence of food. The results obtained with scale-dependant metrics were confirmed by those obtained with scale-independent analyses. Both unveiled the anisotropy of the swimming behavior of grouper larvae that tend to swim toward the vertical axis in order to maximize encounters with prey patches. This study shows that malabar grouper larvae can optimize their search volume by switching their behavior and further draws attention to the need to consider both vertical- and horizontal-projections components while addressing the plankter’s swimming trajectories.     

Swimming behaviour of upriver migrating sea lamprey assessed by electromyogram telemetry

The main subject of this study was the swimming behaviour of upriver migrating sea lamprey, Petromyzon marinus , with particular focus on identification of their swim strategies to overcome areas of difficult passage. A biotelemetry technique (electromyogram telemetry) was used to register muscle activity of the tagged animals. In the 2005 spawning season, five adult sea lampreys were surgically tagged and released in the field. Before release, electromyogram (EMG) records were calibrated with the P. marinus swimming speed in a swim tunnel. Differences between ground speed and swimming speed in the wild suggest that the calibrated CEMG (coded electromyogram) transmitter output corresponds to an activity index, and cannot be properly related to actual swimming speed. This study notes the need to confirm the laboratory calibration curves, to ascertain their use in determining swimming speed of tagged fish in the wild. In 2006, in order to confirm the field results seven adult sea lampreys were tagged, calibrated in the laboratory and released in a 30-m long experimental outdoor canal. The results were similar: observed swimming speed was generally higher when compared with the swimming speed obtained with the EMG signal. In the river, when swimming through slow-flow stretches, sea lampreys maintained a constant pattern of activity, attaining an average ground speed of 0.76 BL s⁻¹ (2.5 km h⁻¹). When sea lampreys encountered rapid flow reaches they alternated between short movements ( c. 67 s) and periods of rest ( c. 99 s). In each swim bout they progressed approximately 14 m; to overcome more difficult obstacles sea lampreys increased their number of burst movements instead of longer or more violent swimming events. About 43% of the time negotiating difficult passage areas was spent in resting by attaching motionless to the substrate with their oral disk.     

Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager

It is widely held that when predator avoidance conflicts with other activities, such as feeding, avoidance of predators often takes precedence. In this study, we examine how predation risk and food distribution interact to influence the schooling behavior and swimming speed of foraging juvenile walleye pollock, Theragra chalcogramma. Fish were acclimated to either spatially and temporally clumped, or spatially and temporally dispersed food for 3 weeks. Fish were then monitored while feeding in the absence and presence of predatory sablefish, Anoplopoma fimbria. Fish foraging for clumped food swam rapidly in a loose school when predators were absent, but swam more slowly and adopted more cohesive schooling in the presence of predators, trading-off foraging opportunity for decreased vulnerability to predators. Fish foraging for dispersed food swam about slowly and did not engage in cohesive schooling in either the absence or presence of predators. These fish accepted greater predation risk in order to continue foraging, suggesting that the cost of schooling, in terms of decreased foraging opportunity, was greater when food was dispersed than when it was clumped. This lower responsiveness to predators among fish receiving dispersed food demonstrates that predator avoidance does not always take precedence over other activities, but rather, that a balance is maintained between predator avoidance and feeding, which shifts as food distribution changes.     

Junk-food in marine ecosystems

The abundance and availability of food are critical determininants of reproductive success and population dynamics of marine top predators. However, recent work has indicated that the quality of the food may also be critically important for some marine predators. The 'junkfood hypothesis' was originally suggested as a potential explanation for a dramatic population decline of Stellers sea lions Eumetopias jubatus in the Gulf of Alaska. According to the hypothesis, a dietary switch to prey of low energy content led to detrimental effects on the population of sea lions. A number of observations indicate that the hypothesis is relevant for several population parameters. Recent work on piscivorous seabirds has provided substantial evidence indicating the relevance of this hypothesis in food webs in e.g. the North Pacific, the North Sea and the Baltic Sea. The emergence of 'junk-food' in these systems may be coupled to large scale changes in climatological and oceanographic forcing, although predation, fishing and competition provide additional plausible hypotheses. It may be possible to predict which kinds of animals will be particularly sensitive to food quality; these seem to be species with limited ability to carry food loads, with energetically-expensive foraging behaviour, and with digestive anatomy evolved to minimize mass at the cost of digestive efficiency. This review suggests that the junk-food hypothesis is a highly relevant factor in relation to sustaining ecosystem resilience, and is an important consideration in ecosystem management. Sustaining healthy populations of marine top-predators requires an understanding of the role of food quality, in addition to food abundance and availability.     

The effect of predation risk on the predatory behaviour of a sit-and-wait predator,Ranatra dispar (Heteroptera: Nepidae), the water stick insect

Two primary defence behaviours, fore-leg extension to enhance crypsis and swimming to bottom and remaining motionless, of a predatory water bug,Ranatra dispar, are described along with their subsequent effect on foraging behaviour. It was hypothesised that hungry predators would respond less and for a shorter duration compared with recently fed individuals when exposed to a model threat stimulus, thereby tending to take a higher risk of predation during feeding than satiated animals. A greater proportion of animals responded overall with the leg extension response compared with the swimming response, although the mean duration of the former was significantly shorter than the latter response. A significantly higher proportion of nonfasted predators responded, and for a longer duration than fasted individuals. The type of model used significantly effected the proportion of animals that responded with leg extensions but not on its duration. In contrast, both number of animals and the duration of the swim/motionless behaviour were significantly effected by stimulus type. The subsequent effect of these 2 behavioural responses on feeding behaviour was examined and showed that although about the same number of predators removed prey from their mouthparts during both responses, significantly more prey were dropped, and therefore lost, during swimming. The results clearly indicate the significant effects that defensive behaviours have on time budgets in foraging behaviour.     

Sea hares use novel antipredatory chemical defenses

Numerous studies have demonstrated that chemical defenses protect prey from predation and have often assumed that these defenses function by repelling predators. Surprisingly, few have investigated the mechanisms whereby predators are affected by these defenses. Here, we examine mechanisms of chemical defense of sea hares (Aplysia californica), which, when attacked by spiny lobsters (Panulirus interruptus), release defensive secretions from ink and opaline glands. We show that ink-opaline facilitates the escape of sea hares by acting through a combination of novel and conventional mechanisms. Ink-opaline contains millimolar quantities of amino acids that stimulate chemoreceptor neurons in the spiny lobster's nervous system. Ink stimulates appetitive and ingestive behavior, opaline can elicit appetitive behavior but can also inhibit ingestion and evoke escape responses, and both stimulate grooming. These results suggest that these secretions function by "phagomimicry," in which ink-opaline stimulates the feeding pathway to deceive spiny lobsters into attending to a false food stimulus, and by sensory disruption, in which the sticky and potent secretions cause high-amplitude, long-lasting chemo-mechanosensory stimulation. In addition, opaline contains a chemical deterrent that opposes appetitive effects. Thus, chemical defenses may act in more complex manners than palatability assays of prey chemistry may suggest.