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Honey gouramis (Trichogaster chuna) received chemical alarm cues derived from conspecific epidermal tissue and, simultaneously, the vocalization produced by a heterospecific gourami species, the sparkling pygmy gourami (Trichopsis pumila). Control trials paired water with the vocalization. In trials that received alarm cues, honey gouramis significantly increased activity relative to control trials that received water, suggesting an attempt to flee and search for refuge. When the recording of the vocalization was later replayed to test fish without any additional chemical cue, fish that had previously experienced alarm cue froze while those that had received water with the vocalization did not change their behaviour. These data indicate that honey gouramis recognize and respond to chemical alarm cues, making this report the second anabantoid species to be recorded with this response. Second, these data indicate that honey gouramis can associate risk of predation with a novel auditory stimulus, including vocalizations from other species. These data suggest the potential for vocalizations to evolve into alarm signals in this group of fishes. This article is protected by copyright. All rights reserved.

Epidermal club cells (ECCs), along with mucus cells, are present in the skin of many fishes, particularly in the well-studied Ostariophysan family Cyprinidae. Most ECC-associated literature has focused on the potential role of ECCs as a component of chemical alarm cues released passively when a predator damages the skin of its prey, alerting nearby prey to the presence of an active predator. Because this warning system is maintained by receiver-side selection (senders are eaten), there is want of a mechanism to confer fitness benefits to the individual that invests in ECCs to explain their evolutionary origin and maintenance in this speciose group of fishes. In an attempt to understand the fitness benefits that accrue from investment in ECCs, we reviewed the phylogenetic distribution of ECCs and their histochemical properties. ECCs are found in various forms in all teleost superorders and in the chondrostei inferring either early or multiple independent origins over evolutionary time. We noted that ECCs respond to several environmental stressors/immunomodulators including parasites and pathogens, are suppressed by immunomodulators such as testosterone and cortisol, and their density covaries with food ration, demonstrating a dynamic metabolic cost to maintaining these cells. ECC density varies widely among and within fish populations, suggesting that ECCs may be a convenient tool with which to assay ecoimmunological tradeoffs between immune stress and foraging activity, reproductive state, and predator–prey interactions. Here, we review the case for ECC immune function, immune functions in fishes generally, and encourage future work describing the precise role of ECCs in the immune system and life history evolution in fishes.

(1) Predation selects for antipredator competence in prey. For fishes with parental care, brood predators exert selection on the morphological phenotype of offspring, and also exert strong selection pressure to promote parental care behavior of adults. (2) This review summarizes field and lab studies on the ontogeny of antipredator competence in convict cichlids, a freshwater fish with extended biparental care of their free-swimming young. (3) Here, data show that differences in swimming performance between small and large young are exploited by parents when they adopt (smaller) young. Velocity and acceleration of startle responses improves nonlinearly with body size, increasing rapidly at a point when the skeleton rapidly ossifies from cartilage to bone, at the size at which discrimination by adopting parents shifts, and the timing of change in the rate of change in area protected by parents. Convict cichlids in a Nicaraguan lake population showed a similar correlation among these traits, but these traits are delayed relative to Costa Rican fish. (4) Population divergence is likely explained by relatively more intense brood predation in the lake, which selects for different optima of larval antipredator competence and parental brood defense.

In Focus: Bairos-Novak, K.R., Ferrari, M.C.O., & Chivers, D.P. (2019). A novel alarm signal in aquatic prey: Familiar minnows coordinate group defences against predators through chemical disturbance cues. Journal of Animal Ecology, 88, 1281-1290, https://doi.org/10.1111/1365-2656.12986. Chemicals released during predation have long been studied as cues to nearby prey that predators are active in the vicinity. Until now, these chemicals have been labelled as cues because there was no compelling evidence for the necessary components of a communication system, namely (a) voluntary control of release of information, (b) capacity for graded responses and (c) the presence of specialized structures for the production and release of the signal. New findings by Bairos-Novak, Ferrari, and Chivers (2019) show that fathead minnows alter the potency of disturbance "cues" when in the presence of other fathead minnows compared to when they are alone and produce either more or different disturbance "cues" when in the presence of familiar conspecifics compared to when they are in the presence of unfamiliar conspecifics. The behavioural response to these cues is shoaling, which would confer fitness benefits to the sender, thereby qualifying as a signal rather than a cue. This is a significant advancement in the field of chemical ecology of aquatic organisms because disturbance "cues" by fathead minnows bear two of the three hallmarks of an incipient disturbance "signal".

Male Red-winged Blackbirds (Agelaius phoeniceus) have red epaulets that are used as badges for intrasexual competition for territory acquisition and defense. Red epaulets reflect very litt...

Chemical cues released as a by-product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme-linked immunosorbent assay (ELISA) revealed whole-body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g-1 ) than control fish (1.5 ± 0.7 ng g-1 ). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.

In a field study of Leon Springs pupfish Cyprinodon bovinus, two questions about female promiscuity were investigated. First, were females selective in the males with whom they spawned or were they unselective, spawning randomly among males? Second, how promiscuous were the females, i.e. with how many males did they spawn? If simply spawning with many males maximized a female's reproductive success, then females might be expected to spawn randomly with as many males as possible. Alternatively, if females were selective but engaged in multiple mating, they would limit their spawning to preferred males. In the only wild population of this endangered fish, breeding males defend closely associated territories in the shallow margins of a single desert pool. No territories were observed elsewhere in the pool. Therefore, all territorial males were present simultaneously and females could survey all of them, depositing any number of eggs with one, a few or many males. Rather than spawning randomly, females surveyed many males first, visited relatively few males and ultimately spawned with a small fraction of those available males. With increasing numbers of spawns, however, females increased the number of different mates with whom they spawned. Thus, females showed a bet-hedging tactic of having a narrow mate preference while also laying eggs in the territories of other males, possibly to reduce egg predation and to avoid inbreeding.

Mobile young under parental care have a high potential for intermixing with other broods, which potentially increases the costs to the foster parents. Here, we examined for the first time the genetic composition of wild-caught broods of the convict cichlid (Amatitlania siquia), a socially monogamous biparental fish, for evidence of brood mixing and adoption. Our microsatellite genotyping data revealed that 79% of broods contained adopted young. Moreover, 25% of broods contained adopted sibsets likely arising from extra-pair matings, a phenomenon hitherto not documented for this species. Overall, adopted foreign fry and host fry in mixed broods were generally different in body length, as would be expected if they have different parents. However, fry from possible extra-pair matings were similar in body length to host fry, suggesting that they are of similar age. Our results are important because they reveal a very high prevalence and degree of brood mixing, and indicate that social monogamy does not necessarily lead to genetic monogamy in the convict cichlid in nature. These findings raise questions about potential brood-mixing mechanisms and the reproductive ecology (especially opportunities for polygamy in nature) of this important model species in the study of animal behaviour.

Individual zebrafish Danio rerio were assayed for exploratory tendency in a serial open field test before and after being maintained on one of four diet treatments that differed in ration and in predictability of food delivery. Danio rerio became more exploratory after being maintained on a diet with a predictable delivery schedule. There was no effect of ration. Thus, exploratory behaviour is inducible by environmental influences independent of genetic predisposition or social interactions. These results have implications for management of correlated behavioural syndromes of exploratory and boldness of animals reared in captivity for later release into wild populations.

Parental investment in unrelated offspring is potentially maladaptive but may be promoted by natural selection if the presence of foreign young enhances the survival of the parents' own young. We experimentally augmented broods of free-ranging convict cichlids (Cichlasoma nigrofasciatum) to test whether survival of the adopting parents' young (fry) increases, in relation to that of control broods, after the addition of smaller foreign fry, and whether such an increase can be attributed to the effect of brood dilution acting alone or to a combination of brood dilution and the effect of differential predation on adopted young. Total fry survival did not differ between experimental (E) broods and control (C) broods, but E broods had significantly more large (host) fry after 5 days and 10 days than C broods did. In E broods, small (foreign) fry suffered higher rates of predation than large fry, indicating differential predation. In E broods starting at 7.0 and 7.5 mm standard length (SL), observed fry mortalities did not differ significantly from mortalities expected from the effect of brood dilution. However, E broods starting at 8.0 mm SL had significantly lower mortalities than expected, indicating that parents that adopt smaller foreign fry can increase the survival of their own fry by the combined effects of brood dilution and differential predation. Within E broods, growth of smaller foreign fry was significantly slower than that of larger host fry, suggesting that intra-brood agonistic behaviour affects access to food for smaller fry. Therefore, increased predation and reduced growth are two negative effects that act on fry of donor parents.

In this study we tested the effects of predation risk on reproductive behaviour of Iowa darters (Etheostoma exile). We recorded the frequency of courtship behaviour (head shaking) and spawning acts for 30 min before and after removing an opaque barrier to expose groups of darters to (1) an empty tank (the before-pike treatment), then (2) a tank containing a pike (the pike treatment), and finally (3) an empty tank (the after-pike treatment). In response to the pike, darters performed significantly less reproductive behaviour than before exposure to the pike. Furthermore, darters performed proportionally less reproductive behaviour in the area in the immediate vicinity of the pike where risk of predation was highest. However, darters continued to occupy the risky area while exposed to the pike. Removal of the barrier in the absence of the pike (the before- and after-pike treatments) had no effect on the overall level of reproductive behaviour, the proportion of reproductive behaviour performed in the immediate vicinity of the pike tank (the risky area), or use of the risky area.

Epidermal club cells of fishes in the superorder ostariophysi have puzzled evolutionary biologists because they were historically linked to chemical alarm signalling and relied on group selectionist explanations. Alternative hypoth- eses to explain the existence of these cells include the possibility of an anti-pathogenic or anti-parasitic function. If this is so, individual fish should invest in increased numbers of club cells after exposure to parasites, and club cells should contain components that reduce the infectivity of skin-penetrating larvae. Infectivity of cercariae of the trematode Ornithodiplostomum sp. was significantly reduced when exposed to the skin extract of fathead minnows (an ostariophysan), but also to skin extract of mollies (a non-ostariophysan that lacks club cells), respectively, compared to controls. Moreover, club cell density was not affected by exposure to cercariae. Taken together, these results are inconsistent with an anti-parasite function for these cells and instead suggest a generic role in response to injury. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 884-890. ADDITIONAL KEYWORDS: alarm substance - anti-predation - Ornithodiplostomum - Ostariophysi - infectivity - Pimephales.

A behavioral syndrome is a suite of behaviors correlated across multiple social contexts. In this study, boldness in the face of predation risk was assessed twice in fish across two different sensory modalities in both the field and lab to ascertain the biological relevance and complexity of this attribute. Individual fathead minnows were captured from a natural field population using traps that either contained chemical alarm cues (conspecific skin extract) or control (well water) and their responses to the presence of predator behind a glass partition assessed in the laboratory. Although fewer fish were captured in alarm cue-labeled traps, these bold fish performed longer predator inspections than shy fish captured in control traps. Thus, a shy/bold behavioral syndrome was expressed consistently across field and lab settings in response to both chemical and visual indicators of danger. Shy and bold individuals did not differ in sex, body length, secondary sexual characteristics, or parasite load but were of more robust physical condition.

Fathead minnows Pimephales promelas exposed to cercariae of the trematode Ornithodiplostomum sp. incurred a significant mass loss 17 days after exposure to 20 or 120 cercariae. Parasite-naive P. promelas showed no evidence of innate recognition or avoidance of cercariae. After a single exposure to cercariae, however, fish responded to chemical and visual cues of dead (thawed) cercariae with a reduction in activity. Encounter rate with cercariae, and hence infection rate, increased with fish activity. The data indicated that experienced P. promelas associated parasitism risk with novel chemical and visual cues that later triggered avoidance behaviour. Parallels and interactions between antiparasite behaviour and antipredator behaviour open new avenues for behavioural ecological research in risk-sensitive decision-making.

Fishes such as minnows in the superorder Ostariophysi possess specialized alarm substance cells (ASC) that contain an alarm cue. Alarm substance can only be released by damage to the epidermis; thus, the release of alarm substance is a reliable indicator of predation risk. When nearby minnows detect the cue, they adopt a range of antipredator behaviors that reduce their probability of predation. Predator–predator interactions afford prey an opportunity to escape and, thus, a fitness benefit that maintains alarm substance calls over evolutionary time. Here, we present data from a simple field experiment verifying that nearby predators are attracted to minnow alarm substance because it signals an opportunity to pirate a meal. Fishing lures were baited with sponge blocks scented with either (1) water (control for sponge odor and appearance), (2) skin extract from non-ostariophysan convict cichlids (superorder Acanthopterygii, Archocentrus “Cichlasoma” nigrofasciatus) to control for general injury-released cues from fish, or (3) skin extract from fathead minnows (superorder Ostariophysi, Pimephales promelas). Predator strike frequency on each sponge type was 1,1, and 7 for water, cichlid, and minnow cues, respectively. These data provide the first field test using fish predators of the predator-attraction hypothesis for the evolution of Ostariophysan alarm substance cells.

Injury-released chemical cues are reliable indicators of predation risk among many aquatic taxa. When a novel, neutral stimulus is presented in tandem with chemical cues from an injured conspecific, an association is formed between the novel stimulus and apparent risk. Learned recognition of predation risk is well documented for fathead minnows, Pimephales promelas. When minnows detect alarm cues in nature they are also potentially exposed to multiple environmental stimuli, few of which are likely to be relevant indicators of risk. How do minnows discern among candidate stimuli potentially associated with predation risk? Two possibilities are shape and motion. In this study, individual piscivore-naive minnows were presented simultaneously with conspecific chemical alarm cues and two stimulus objects. One object was a darkened tube with its long axis in the horizontal plane (fish-like). The second object was a black disk. Following introduction of chemical alarm cues, one of the objects was raised and lowered repeatedly. After a single conditioning trial, minnows associated risk significantly more with the previously moving object than the previously stationary object, as indicated by reduced activity. Object shape had no significant effect on response intensity in test trials. Our data suggest that minnows have been selected to form aversive responses to moving objects at a site of recent predation because movement is a more predictable indicator of predator identity than shape.

Fathead minnows (Pimephales promelas) adopt antipredator (alarm) behavior when they detect alarm pheromone released from an injured conspecific. This is an adaptive response since alarm pheromone is generally released only in the context of a predation event. Alarm reactions may also occur in response to chemical and visual stimuli that minnows learn to associate with release of alarm pheromone. Here, we tested if fathead minnows can learn to associate a nonbiological, visual stimulus with predation risk. Minnows were simultaneously exposed to red light and conspecific alarm pheromone, inducing an alarm reaction. When retested using red light alone, small shoals of minnows displayed an antipredator response: dashing movements and disorganized swimming followed by decreased height in the water column and increased shoal cohesion. This resulted from a single-trial exposure to the combined cues and demonstrates a robust ecological mechanism by which minnows learn to recognize indicators of predation risk that may vary in space and time. However, learning to associate risk with biologically irrelevant stimuli may be an ecological liability. How minnows discern between relevant and irrelevant stimuli in nature is not known.

A re-examination of data from Wisenden & Smith Journal of Fish Biology50, 799–808) suggests that fathead minnows Pimephales promelas adjust investment into epidermal alarm substance cells (ASC) facultatively based upon the level of perceived risk. When placed into a container with non-familiar shoalmates (relatively high risk) ASC production increased. This allows these individuals to attract a secondary predator better. When placed into a container with familiar shoalmates (relatively low risk) ASC production decreased. This may reflect increased effectiveness of a group antipredator response by familiar individuals, and/or the cost to inclusive fitness of attracting additional predators to the vicinity of their kin.

SYNOPSIS. Sexual selection theory predicts a coevolution between male sexual ornamentation and female preference. The implication of this prediction for sensory ecology is that there should be a tight coupling between the physiology of male signal production and the physiology of female signal reception. Indicator models of sexual selection predict that male ornamentation is correlated with male condition, and that female preference is correlated with male ornamentation. Indicator models of sexual selection have a conceptual overlap with resource acquisition and investment models of behavioral ecology. Empirical studies with fishes, particularlywith guppies ( Poecilia reticulata ) and threespine sticklebacks ( Gasterosteus aculeatus ), suggest a strong connection between acquired resources, male condition, male ornamentation, male courtship, and female preference.

We tested the explanatory value of two hypotheses reviewed by Lack (1954) in the maintenance of brood size in free-ranging convict cichlidsCichlasoma nigrofasciatum: (1) physiological constraints on egg production, and (2) behavioural constraints imposed by brood defence. Number of free-swimming young in 13 experimental (E) broods was augmented to the upper limit of the size distribution of natural broods (150 young); 18 control (C) broods were handled in the same way but brood size was not changed (mean ± SE = 69.5 ± 11.0). E and C brood sizes were measured at 5 day intervals. At day 20 (just before independence from parental care), 50.3 ± 9.4 (n = 9) young remained in E broods and 30.8 ± 7.8 (n = 8) young remained in C broods (p> 0.05). Offspring number did not differ significantly (p> 0.05) between C and E broods after day 10. Mean growth rate of offspring was significantly lower in E broods than in C broods, perhaps in response to increased density of young in the former. Both the convergence of offspring number in E and C broods and suppression of growth in E broods support a behavioural constraint; that during the first 10 days in which the young are free swimming, two parents are unable to defend large broods as successfully as small broods. A trade-off exists in parental investment between current and future reproduction. Extra-parental investment in current reproduction (eggs) does not result in an increased number of young at independence, therefore a behavioural constraint during brood defence should stabilize the evolution of clutch size.

In fish, the predominant form of parental care is brood defence. The convict cichlid, a biparental fish native to Central America, also engages in two types of brood provisioning: fin digging and leaf lifting. These behaviour patterns were studied in the field, and in outdoor experimental ponds and laboratory aquaria. In the ponds, females fin dug 51 times more often when guarding fry than when unmated; males fin dug three times more frequently when guarding fry than when unmated. After the young became free-swimming, females performed four times (field) and two times (pond and laboratory) more fin digging and twice as many leaf lifts (field) as males. Females in the field increased leaf lifting with brood age but males did not. Fin digging frequency by parental females and males increased with brood age. Frequency of adult feeding bites at the substrate did not change with brood age except in the field, where female feeding bites increased with brood age. In the field, females performed more feeding bites than males but in the laboratory males fed more often than females. Thus changes in fin digging frequency with brood age do not seem to be strongly linked to the feeding requirements of the parents. In the laboratory, fin digging frequency was influenced by substrate quality ( P = 0·08) but not by ration ( P > 0·10). Taken together, these data support the hypothesis that parental fin digging and leaf lifting help increase food availability to their young.

Parental care theory predicts that investment in current reproduction should be increased when the prospects of success in current reproductive effort are relatively high, and reduced when they are poor relative to expected success from future reproductive effort. A number of studies have shown that levels of postspawning parental investment (brood defence, parents' willingness to risk predation) increase when the brood is augmented. However, few studies have shown a change in pre-spawning (gonadal) investment in response to indirect indicators of reproductive success, such as nest site quality. Convict cichlids (Cichlasoma nigrofasciatum) are small freshwater fish that have biparental care of their young. Pairs of convict cichlids were required to spawn in either "risky" or "secure" spawning caves in the presence of potential egg predators. As predicted by parental care theory, females laid significantly more eggs in secure spawning caves than in risky spawning caves. The ability of this iteroparous fish to adjust gonadal investment in this manner would serve to optimize the use of its resources under varying environmental conditions and ultimately allow it to realize maximize lifetime reproductive success.

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica ), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia . These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator–prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.

Convict cichlids (Cichlasoma nigrofasciatum) are biparental, substrate brooding cichlid fish which have extended care of their eggs, larvae (wrigglers) and free-swimming young (fry). Field observations indicate that intraspecific brood adoption of fry occurs frequently under natural conditions. Of 232 broods 29% contained foreign fry and of 232 broods 15% were identified as fry donors. Foreign fry were usually of similar size to or smaller than the host brood fry. Experimental fry transfers showed that parents accept foreign fry smaller than their own but immediately reject or eat foreign fry larger than their own. A predation experiment showed that within a mixed brood, smaller fry are eaten more often than larger fry. Thus, accepting foreign fry may benefit parents through the dilution effect and through a differential predation effect. In comparison with intact families, broods from which the male parent was removed were less likely to reach independence, had fewer fry surviving to independence, and had a greater probability of having some fry transferred to neighbouring broods. We propose that intraspecific brood adoption in convict cichlids is mutually beneficial to the adult donors and recipients.