A multi-phylum study of grazer-induced paralytic shellfish toxin production in the dinoflagellate Alexandrium fundyense: A new perspective on control of algal toxicity

The present study surveyed grazer-induced stimulation of paralytic shellfish toxin (PST) production by the marine dinoflagellate Alexandrium fundyense. The survey included species, known to graze upon A. fundyense, from five phyla: the protists, Polykrikos kofoidii (Dinoflagellata) and Tiarina fusus (Ciliophora), the bivalve molluscs Mytilus edulis and Mya arenaria (Mollusca), the ascidians, Molgula manhattensis and Botrylloides violaceus (Chordata), and the copepod, Eurytemora herdmani (Arthropoda). Direct (grazers in contact with cells of A. fundyense) and indirect (grazers not in contact with cells of A. fundyense) induction assays were carried out with protists and copepods. Only indirect assays were carried out with molluscs and ascidians. Indirect assays also tested whether induction of PST production occurred via kairomones or feeding-related cues. All metazoan grazers induced PST production. By contrast, neither of the two species of protistan grazer induced PST production. Direct and indirect inductions of PST production were evident for the copepod, with direct induction being significantly higher than indirect induction. Effects upon PST production by phylum, species (nested within phylum), and interactions of phylum by diet, and species by diet, were evident. When induction of PST production occurred, a kairomone effect was apparent, except for M. edulis. Similarly, feeding-related cues were evident, except for E. herdmani. An asymptotic relationship between the magnitude of indirect induction of PST production and total cell ingestion by the grazers suggests a saturation response of grazer-induced PST production.     

Cell-growth gene expression reveals a direct fitness cost of grazer-induced toxin production in red tide dinoflagellate prey

Induced prey defences against consumers are conspicuous in microbes, plants and animals. In toxigenic prey, a defence fitness cost should result in a trade-off between defence expression and individual growth. Yet, previous experimental work has failed to detect such induced defence cost in toxigenic phytoplankton. We measured a potential direct fitness cost of grazer-induced toxin production in a red tide dinoflagellate prey using relative gene expression (RGE) of a mitotic cyclin gene (cyc), a marker that correlates to cell growth. This approach disentangles the reduction in cell growth from the defence cost from the mortality by consumers. Treatments where the dinoflagellate Alexandrium catenella were exposed to copepod grazers significantly increased toxin production while decreasing RGE of cyc, indicating a defence-growth trade-off. The defence fitness cost represents a mean decrease of the cell growth rate of 32%. Simultaneously, we estimate that the traditional method to measure mortality loss by consumers is overestimated by 29%. The defence appears adaptive as the prey population persists in quasi steady state after the defence is induced. Our approach provides a novel framework to incorporate the fitness cost of defence in toxigenic prey–consumer interaction models.     

Induction of toxin production in dinoflagellates: the grazer makes a difference

The dinoflagellate Alexandrium minutum has previously been shown to produce paralytic shellfish toxins (PST) in response to waterborne cues from the copepod Acartia tonsa. In order to investigate if grazer-induced toxin production is a general or grazer-specific response of A. minutum to calanoid copepods, we exposed two strains of A. minutum to waterborne cues from three other species of calanoid copepods, Acartia clausi, Centropages typicus and Pseudocalanus sp. Both A. minutum strains responded to waterborne cues from Centropages and Acartia with significantly increased cell-specific toxicity. Waterborne cues from Centropages caused the strongest response in the A. minutum cells, with 5 to >20 times higher toxin concentrations compared to controls. In contrast, neither of the A. minutum strains responded with significantly increased toxicity to waterborne cues from Pseudocalanus. The absolute increase in PST content was proportional to the intrinsic toxicity of the different A. minutum strains that were used. The results show that grazer-induced PST production is a grazer-specific response in A. minutum, and its potential ecological importance will thus depend on the composition of the zooplankton community, as well as the intrinsic toxin-producing properties of the A. minutum population.     

Grazing on a toxic Alexandrium catenella bloom by the lobster krill Munida gregaria (Decapoda: Galatheoidea: Munididae)

Specimens of Munida gregaria were collected within and in the vicinity of a bloom of the toxic dinoflagellate Alexandrium catenella in Queen Charlotte Sound, New Zealand. The crustacean contained paralytic shellfish toxin (PST) with an analogue profile dominated by N-sulfocarbamoyl analogues (C1,2 and GTX5) and carbamate gonyautoxins (GTX1,4), similar to that of the dinoflagellate. A feeding experiment showed that M. gregaria is capable of actively grazing on A. catenella and it may play a role in controlling population growth of the dinoflagellate. This is the first account of the accumulation of PST by M. gregaria. When it is periodically abundant, M. gregaria is an important food item for fish, birds and other marine fauna and they are a vector by which PST may be transferred to higher trophic levels.     

Determining sensitive stages for learning to detect predators in larval bronzed frogs: Importance of alarm cues in learning

Successful survival and reproduction of prey organisms depend on their ability to detect their potential predators accurately and respond effectively with suitable defences. Predator detection can be innate or can be acquired through learning. We studied prey–predator interactions in the larval bronzed frogs (Sylvirana temporalis), which have the innate ability to detect certain predators. We conducted a series of experiments to determine if the larval S. temporalis rely solely on innate predator detection mechanisms or can also learn to use more specific cues such as conspecific alarm cues for the purpose. The results of our study clearly indicate that larval S. temporalis use both innate and learned mechanisms for predator detection. Predator-naïve tadpoles could detect kairomones alone as a potential threat and responded by reducing activity, suggesting an innate predator detection mechanism. Surprisingly, predator-naïve tadpoles failed to detect conspecific alarm cues as a potential threat, but learned to do so through experience. After acquiring the ability to detect conspecific alarm cues, they could associate novel predator cues with conspecific alarm cues. Further, post feeding stages of larval S. temporalis are sensitive for learning to detect conspecific alarm cues to label novel predators.     

Modelling paralytic shellfish toxins (PSTs) transfer and accumulation in populations of two planktonic grazers

A model was developed in this paper in order to study and compare the paralytic shellfish toxin (PST) transfer and accumulation of two different potential PST vectors in the planktonic community, the heterotrophic dinoflagellate in its red form Noctiluca scintillans and the copepod Acartia clausi. Different factors that influence the toxin transfer such as toxin synthesis, grazing on toxic and non-toxic food and population size of PST producers and vectors were considered in the model. Moreover, a laboratory experiment was conducted in order to calculate the detoxification rates of Noctiluca fed on Alexandrium catenella. According to the model results, the two grazers showed a significant difference mainly in the timing of the PST accumulation. Noctiluca exhibited a rapid response to the grazing of Alexandrium with high initial toxin accumulation, followed by a reduction to zero concentration of toxins in a period of almost two days. In contrast, Acartia showed a considerable delay in comparison to Noctiluca to accumulate the same amount of toxin in the population. This delay is linked to the slower reproduction rates that characterize the copepod. The range of the initial values used for the sensitivity analysis of the model is representative of the coastal environment of a Galician ria (embayment located at the NW of Iberian Peninsula), where the two grazers and Alexandrium may co-exist. The model for Acartia showed less sensitivity to these key parameters probably due to the time delay in accumulation of significant amount of toxins. Both grazers showed a rapid (50 h) reduction of ingested toxin, suggesting inefficiency to transfer toxins through predation in the food web.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus

Predation imposes selection on the ability of prey to recognize and respond to potential threats. Many prey species detect predators via chemoreception, particularly in aquatic environments. Also, chemical cues from injured prey are often perceived as an indication of predation risk. However, because antipredatory behavior can be costly, prey responses should depend on the current level of risk that each predator poses, which may depend on the type of chemical cues detected. We exposed larval newts, Triturus pygmaeus, to chemical cues from predator larval beetles or to alarm cues from conspecific larval newts and examined the behavioral changes of larval newts. Results showed that larval newts reduced activity levels when conspecific alarm cues were present but not when the predator cues alone were present. These results might suggest that larval newts are unable to recognize predator chemicals. To avoid costs of unnecessary antipredatory behaviors, larval newts may benefit by avoiding only predators that represent a current high level of threat, showing only antipredatory responses when they detect conspecific alarm cues indicating that an actual predatory attack has occurred.     

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, <Emphasis Type="Italic">Umbra limi</Emphasis> (Kirtland 1840)

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory.     

Is there a fish alarm cue? Affirming evidence from a wild study

Chemical alarm cues released from injured tissue are not released under any other context and therefore reliably inform nearby prey of the presence of a predator. Laboratory and field studies have demonstrated that most aquatic taxa show antipredator responses to chemical alarm cues. Ostariophysan fish (e.g. minnows) possess specialized skin cells that contain an alarm chemical. Magurran et al. (1996, Proceedings of the Royal Society of London, Series B,263, 1551-1556) were the first to use underwater video to carefully document the behavioural response of free-ranging wild populations of minnows to minnow alarm cues. They found no evidence of an antipredator response, and challenged the assumption that the contents of these cells indicate risk in the field. They proposed that alarm responses are context dependent in that they are an artefact of enclosed environments such as laboratory aquaria and field traps. Here, we repeat their experiment on free-swimming field populations of littoral fish and report a significant decrease in the number of fish in areas where chemical alarm cues of blacknose shiners, Notropis heterolepis (Ostariophysi: Cyprinidae) were released. The effect of these chemical cues was equal in magnitude to the effect of the presentation of a model predator. The response to the approach of a model predator (visual cue) was intensified by pre-exposure to chemical alarm cues. We corroborated this interaction between chemical and visual indicators of predation risk in a laboratory study using glowlight tetras, Hemigrammus erythrozonus (Ostariophysi: Characidae). Response to the visual stimulus of a predator was significantly intensified by previous exposure to conspecific chemical alarm cues. We conclude that ostariophysan skin indeed contains an alarm cue that (1) informs nearby prey of imminent predation risk, (2) induces some form of antipredator behaviour in most contexts, and (3) affects subsequent behavioural responses to stimuli in other sensory modalities.     

Detection of cyanobacterial sxt genes and paralytic shellfish toxins in freshwater lakes and brackish waters on Åland Islands,Finland

Harmful cyanobacteria are a globally growing concern. They produce a large variety of toxic compounds, including saxitoxin and its many structural variants, a group of potent neurotoxins collectively called paralytic shellfish toxins or PST. Nucleic acid based detection methods, such as qPCR, have been proposed as potential screening and monitoring tools for toxic cyanobacteria, but it is not clear how well the presence and quantity of saxitoxin biosynthesis (sxt) genes can be used to predict the production of PST in the environment. In this study, the prevalence of three sxt genes and their co-occurrence with paralytic shellfish toxins in the environment was investigated. The sxtA, sxtG and sxtB genes were present on average in 31% of the samples collected from lakes and brackish coastal waters on Åland Islands, Finland, during the three-year monitoring period. PST detection frequency varied from 13% to 59% from year to year, and concentrations were generally low. On average higher sxtB copy numbers were associated with PST detection, and although a positive correlation between gene copy numbers and toxin concentrations was observed (Spearman rank correlation, ρ = 0.53, P = 0.012), sxt gene presence or quantity didn’t reliably predict PST production. Sequencing of sxtA fragments and identification of main cyanobacteria indicated that the likely candidate responsible for PST production in the samples belonged to the genus Anabaena.     

The effects of interspecific competition and prey odor on foraging behavior in the rock crab, Cancer irroratus (Say)

The effects of competitor pressure and prey odor on foraging behavior of the rock crab, Cancer irroratus (Say), were investigated. The Jonah crab, Cancer borealis (Stimpson), was chosen as the interspecific competitor because it shares resources with C. irroratus. Four treatments were tested for their effect on foraging: the presence or absence of a competitor and two types of prey odor; body odor (living mussel) and tissue extract (dead mussel tissue). The presence of Jonah crabs did not influence location time, search time, prey size selected, or handling time of the rock crabs. However, rock crabs responded differently to the presence of body odor and tissue extract cues. The presence of extract odor decreased the time to locate prey while increasing the number of prey manipulated and prey size selected. When prey body odor was present, rock crabs displayed less investigative behaviors than in the presence of extract odor, illustrated by reduced location time. Extract odor provided a stronger and more attractive cue than body odor, but increased prey manipulation and search time. Extract odor induced increases in manipulation and searching for prey but canceled out the benefits of decreased location time, resulting in crabs from both treatments displaying similar search times. These elevated behaviors may be associated with foraging for injured and cracked prey or may indicate an area of conspecific feeding.     

Effects of the toxic dinoflagellate Alexandrium catenella on histopathogical and escape responses of the Northern scallop Argopecten purpuratus

Juvenile Northern scallops Argopecten purpuratus were exposed to cultures of the paralytic shellfish toxin (PST) producing dinoflagellate, Alexandrium catenella, or a non-toxic microalga as a control, T-iso. After 3 and 6 days of exposure to either A. catenella or T-iso, scallops were stimulated to elicit an escape response by exposing them to the predatory sea star Meyenaster gelatinosus. We monitored the escape response of the scallops in terms of reaction time after first contact with the sea star, number of claps (burst of rapid valve closures) until exhaustion, clapping time, clapping rate, the time scallops spent closed when exhausted, and recovery from the initial number of claps, clapping time and clapping rate. Additionally, histopathological and stress responses (through heat-shock protein [hsp70] induction), as well as accumulation of Paralytic Shellfish Poisoning (PSP) toxins, were monitored on scallops after 3 and 6 days of exposure to A. catenella. After 6 days of exposure, scallops exposed to A. catenella accumulated PSTs and reacted more rapidly with a higher clapping rate, however the duration of their escape response was shorter than controls, when exposed to M. gelatinosus. Additionally, scallops exposed to A. catenella showed histopathological features, especially after 6 days of exposure, including increased melanization of the tissues and myopathy, with high levels of degeneration of the muscle fibers. A six-day exposure to A. catenella also caused an increase in prevalence of rickettsiales-like organisms within scallop tissues. This study suggests that PST accumulation can affect the interaction between the Northern scallop and both pathogens and predators, potentially increasing their susceptibility to either of them.     

Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues

The ability to accurately assess local predation risk is criticalto prey individuals, as it allows them to maximize threat-sensitivetrade-offs between predator avoidance and other fitness relatedactivities. A wide range of taxonomically diverse prey (includingmany freshwater fishes) relies on chemical alarm cues (alarmpheromones) as their primary information source for local riskassessment. However, the value of chemical alarm cues has beenquestioned due to the availability of additional sensory inputs(i.e., visual cues) and the lack of an overt antipredator responseunder conditions of low perceived risk. In this paper, we testthe hypothesis that chemical alarm cues at concentrations belowthe point at which they elicit an overt behavioral responsefunction to increase vigilance towards other sensory modalities(i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammuserythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide(the putative Ostariophysan alarm pheromone) did not exhibitan overt antipredator response in the absence of secondary visualcues (not different than the distilled water control). However,when exposed to the sight of a visually alarmed conspecific,they significantly increased the intensity of their antipredatorresponse (not different from shoals exposed to the suprathresholdalarm cue). This study demonstrates that prey may benefit fromresponding to low concentration alarm cues by increasing vigilancetowards secondary cues during local risk assessment, even inthe absence of an overt behavioral response. By increasing vigilancetowards secondary risk assessment cues in the presence of alow risk chemical cue, individuals are likely able to maximizethe threat-sensitive trade-offs between predator avoidance andother fitness related activities.     

Underwater Video Reveals Strong Avoidance of Chemical Alarm Cues by Prey Fishes

A diversity of fishes release chemical cues upon being attacked by a predator. These cues, commonly termed alarm cues, act as sources of public information warning conspecifics of predation risk. Species which are members of the same prey guild (i.e. syntopic and share predators) often respond to one another's alarm cues. The purpose of this study was to discriminate avoidance responses of fishes to conspecific alarm cues and cues of other prey guild members from responses to unknown damaged fish odours and novel odours. We used underwater video to measure avoidance responses of freshwater littoral species, namely fathead minnows (Pimephales promelas), finescale dace (Chrosomus neogaeus), and brook stickleback (Culaea inconstans), to both injured fish cues and novel non‐fish odours. The cyprinids (minnows and dace) showed significant avoidance of minnow cues over swordtail cues, morpholine, and the control of distilled water and tended to avoid fathead cues over cues of known prey guild members (stickleback). Cyprinids also significantly avoided cues of stickleback over unknown heterospecific cues (swordtail) and tended to avoid stickleback cues over morpholine and the distilled water control. Stickleback significantly avoided fathead minnow extract over the distilled water and tended to avoid stickleback and swordtail over distilled water. We conclude that fishes in their natural environment can show dramatic changes in behaviour upon exposure to alarm cues from conspecifics and prey guild members. These responses do not represent avoidance of cues of any injured fish or any novel odour.     

Assessment of Predation Risk by Juvenile Yellow Perch, Perca flavescens: Responses to Alarm Cues from Conspecifics and Prey Guild Members

In two laboratory experiments we tested juvenile yellow perch, Perca flavescens, for behavioural responses to alarm cues of injured conspecifics and several prey guild members: adult perch, Iowa darters, Etheostoma exile and spottail shiners, Notropis hudsonius. Spottail shiners are phylogenetically distant to yellow perch whereas Iowa darters and perch are both members of the Family Percidae. Groups of juvenile yellow perch increased shoal cohesion and movement towards the substrate after detecting conspecific alarm cues when compared to cues of injured swordtails, Xiphophorus helleri, a species phylogenetically distant from perch. Individual juvenile perch increased shelter use and froze more when exposed to chemical alarm cues from both juvenile and adult perch, shiners and darters compared to exposure to injured swordtail cues or distilled water. The response to cues of darters may indicate that alarm cues are evolutionarily conserved within percid fishes or that perch had learned to recognize darter cues. The response to spot tail shiners likely represents learned recognition of the cues of a prey guild member.     

Contribution of several nitrogen sources to growth of Alexandrium catenella during blooms in Thau lagoon,southern France

A monitoring program with a weekly sampling frequency over a 15-month period indicates that urea concentrations above a certain threshold level may trigger the blooms of Alexandrium catenella in Thau lagoon. However, urea concentrations were also sometimes related to ammonium and dissolved organic nitrogen concentrations, indicating that the role of urea may not be a direct one. An original approach is used to assess the relative contribution of several nitrogen sources (nitrate, nitrite, ammonium, urea) to growth of A. catenella by comparing nitrogen uptake rates to nitrogen-based growth rates estimated from dilution experiments during four blooms over a 4-year period (2001–2004) in Thau lagoon. Nitrate and nitrite contributed 0.1–14% and 0.1–5% respectively of growth requirements. Ammonium and urea were the main N sources fueling growth of A. catenella (30–100% and 2–59%, respectively). Indirect estimates indicated that an unidentified N source could also contribute significantly to growth at specific times. Concerning ammonium and urea uptake kinetics, half-saturation constants varied between 0.2 and 20 μgat N L⁻¹ for ammonium and between 0.1 and 44 μgat N L⁻¹ over the 4-year period, indicating that A. catenella can have a competitive advantage over other members of the phytoplankton even under low concentrations of ammonium and urea. However, the observed large changes in ammonium and urea uptake kinetics on a short time scale (days) during blooms preclude more precise estimates of those contributions to growth and require further investigation.     

Friends in Low Places: Responses of a Benthic Stream Fish to Intra‐Prey‐Guild Alarm Cues

Many aquatic species produce chemical alarm cues that serve as a warning to nearby conspecifics. In mixed‐species aggregations, individuals may also benefit by ‘eavesdropping’ on the chemical alarm cues of other species that are in the same prey guild. Rainbow Darters (Etheostoma caeruleum) are benthic fish that co‐occur with native Ozark Minnows (Notropis nubilus), recently introduced Western Mosquitofish (Gambusia affinis), and native Oklahoma Salamanders (Eurycea tyrnerensis), all of whom are vulnerable to the same predators. We tested the responses of darters to the damage‐released alarm cues of conspecifics (positive control), minnows, and mosquitofish; alarm cues from Bumblebee Gobies (Brachygobius doriae) served as a negative (allopatric) control. We also tested the response of sympatric and allopatric darters to the damage‐released alarm cues of Oklahoma Salamander. Darters exhibited a fright response to conspecific and minnow alarm cues, but not to cues from mosquitofish or gobies. Lack of response to mosquitofish cues could be because they are introduced or because they typically occur higher in the water column than darters. Darters that were sympatric with the salamander exhibited a fright response to the alarm cues of the salamander, while allopatric darters did not. Rainbow Darters can develop responses to the alarm cues of syntopic species (minnows and Oklahoma Salamander) within their prey guild.     

Biological interactions in enclosed plankton communities including Alexandrium catenella and copepods: Role of phosphorus

A microcosm approach was used to test whether: a) growth under unbalanced nutrient conditions (varying N:P ratios) affected the susceptibility of a phytoplankton community including the dinoflagellate Alexandrium catenella (a paralytic shellfish toxin producer) to mesozooplankton grazing, and b) the potential effects of unbalanced nutrient conditions were mediated by changes in toxicity of A. catenella or by other mechanisms. The experimental setup consisted of fifteen 30 l microcosms, filled with water from the Barcelona Harbour and subjected to treatments combining nutrient inputs at three different N:P ratios (Redfield N:P ratio or nutrient-balanced, high N:P and low N:P), addition or omission of A. catenella (an estimated initial concentration of 38 A. catenella cells ml^− 1, a value typical for blooms in harbours of the Catalan coast), and selective addition of a cultured population of Acartia grani. P sufficiency had a strong positive effect on the growth of A. grani, both with or without A. catenella addition, presumably due to enhanced food quality of the prey community. The presence of this copepod resulted in lower concentrations of ciliates, A. catenella, and other dinoflagellates, suggesting active grazing by the copepods. No noxious effects of A. catenella on the copepods were detected at the relatively low cell concentrations of that dinoflagellate used in the experiment.     

Cortisol influences the antipredator behavior induced by chemical alarm cues in the Frillfin goby

We evaluated the effect of increased plasma cortisol levels on fish antipredator behavior induced by conspecific chemical alarm cues. The experimental model for the study was the Frillfin goby Bathygobius soporator. We first confirmed that the alarm substance induces typical defensive antipredator responses in Frillfin gobies and described their alarm substance cells (epidermal ‘club’ cells). Second, we confirmed that intraperitoneal cortisol implants increase plasma cortisol levels in this species. We then demonstrated that exogenous cortisol administration and subsequent exposure to an alarm substance decreased swimming activity to a greater extent than the activity prompted by either stimulus alone. In addition, cortisol did not abolish the sheltering response to the alarm chemical cue even though it decreased activity. As predators use prey movements to guide their first contact with the prey, a factor that decreases swimming activity clearly increases the probability of survival. Consequently, this observation indicates that cortisol helps improve the antipredator response in fish.