Alarm responses, fish

Even a neutral chemical cue can trigger alarm responses in fish if they had experienced it together with a true alarm signal. A coral-reef dwelling goby, Asterropteryx semipunctatus, learned to associate a novel chemical cue from a... 

Some taxa may possess pheromone-producing tissues, while others have similar tissues but without pheromones. At the cellular level, extensive comparative studies of fish alarm responses show that cyprinids possess club cells, which release an alarm odor when ruptured by a predator attack. Polypteriformes have... 

Olfaction, the sense of smell, is an important neural system in various animal species, including fish, for their life. Fish can detect a variety of odorants emitted from objects and dissolved in the water, such as amino acids, bile salts, nucleotides, polyamines, prostaglandins, and steroids. The fish olfactory system is extensively developed to receive and discriminate these odorant molecules, to transmit their signals to the brain, and to mediate fundamental behaviors such as food finding, alarm response, predator avoidance, social communication, reproductive activity, and spawning migration (Sorensen and Caprio 1998 Zielinski and Hara 2007). 

The neural pathways mediating alarm responses were examined in the crucian carp (Carassius carassius L.). In these fish, two olfactory tracts convey information from the olfactory bulbs [adjacent to the olfactory organs (i.e., nostrils)] to other parts of the brain. One courses along the midline (the medial olfactory tract) and the other along the side (the lateral olfactory tract). The medial olfactory tract further divides into two bundles (the medial and the lateral bundles of the medial olfactory tract). Severing the medial bundle of the medial olfactory tract eliminated the alarm responses to skin extract, whereas severing the lateral bundle of the medial olfactory tract diminished the feeding behavior (Hamdani et al. 2000). 

Williams (1964, 1992), however, argued that there are considerable problems in explaining the evolution of an alarm pheromone. It was assumed that individuals produced alarm substance to warn their school or species of danger, but schools of fish are not composed of closely related individuals (Naish et al. 1993). Magurran et al. (1996) further demonstrated that fright responses in fish were elicited in a context-dependent manner. The alarm responses were likely exaggerated in the laboratory condition where the opportunities for escape were largely reduced. In the natural environment, alarm substances did not produce adaptive behaviors. In crustaceans, behaviors similar to the alarm response in fish can be elicited by the reception of injured conspecifics (Hazlett, Chap. 18). 

In order to assess the effect of variation in alarm cue concentration on the duration of alarm responses, we calculated the average shoaling index and vertical area use score for each group of fish during the pre-stimulus period to determine a baseline level of response. Following exposure to the stimulus we calculated the shoaling index and vertical area scores for each group of fish for 1 minute intervals of the 8 minute poststimulus period. We used repeated measures ANOVA to determine the effects of treatment on the response of the fish and whether there was a treatment by time interaction. 

The skin of two groups of fish that show alarm responses to skin extract. (A) The skin of an ostariophysan fish, the bluehead chub (Nocomis leptocephalus), illustrating the alarm substance cells (ASCs) in the epidermis (b)... 

Why should ostariophysan fishes differentiate and maintain specialized cells that may constitute over 30% of their epidermis when these cells have no known function other than warning other individuals Explanations for this situation fall into two main categories. What I will term alarm theories are based on some benefit of the alarm signal redounding to improve the fitness of the sender. Non-alarm theories are based on some primary function for the ASCs and their contents that benefits the possessor directly without reference to the alarm response of other individuals. 

In minnows, taste is not sufficient for predator recognition. Anosmic fathead minnows, P. pmmelas, did not show the flight reaction to the odor of northern pike, Esox lucius (Chivers and Smith, 1993). Naive European minnows, Phoxinus phoxinus, do not exhibit a fright reaction when first exposed to a predator odor, such as that of pike, E. lucius. They develop a conditioned fright response only after experiencing the predator odor in dangerous circumstances, such as when accompanied by schreckstoff (alarm pheromone) of conspecifics. Responses to the odor of non-piscivorous fishes such as tilapia, Tilapia mariae, can also be conditioned in this fashion but the responses are much weaker (Magurran, 1989). 

Brown GE, Adrian JC Jr, Kaufman IH, Erickson JL, Gershaneck D (2001) Responses to nitrogen-oxides by chariciform fishes suggest evolutionary conservation in Ostariophysian alarm pheromones. In Marchlewska-Koj A, Lepri J, Muller-Schwarze D (eds) Chemical signals in vertebrates. Plenum, New York, pp 305-312... 

Decrease in pH in the water have been shown to affect the responses to alarm cues in fish either due to suggested changes in the molecules themselves (e.g. Leduc et al. 2004) or possibly due to effects on the olfactory receptors (Thommesen 1983). 

McPherson TD, Mirza RS, Pyle GG (2004) Responses to wild fishes to alarm chemicals in pristine and metal-contaminated lakes. Can J Zool 82 694-700... 

My goal in this paper is to briefly describe the role of chemical alarm cues in local risk assessment, focusing on threat-sensitive trade-offs. Specifically, I will address the following questions (1) do prey fish show graded responses in overt antipredator responses with decreasing stimulus concentration, (2) are prey fish able to detect chemical alarm cues below their minimum overt behavioural response threshold, and (3) do prey fish exhibit threat-sensitive changes in behaviour in response to alarm cues at concentrations below the minimum overt response threshold ... 

Brown, G. E., Adrian, J. C. Jr., Kaufinan, L H., Erickson, J. L., and Gershaneck, D, 2001b, Responses to nitrogen-oxides by Characiforme fishes suggest evolutionary conservation in Ostariophysan alarm pheromones, in Chemical Signals in Vertebrates, Vol. 9, A. Marchlewska-Koj, J.J. Lepri, and D. MOller-Schwarze, eds.. Plenum Press, New York, pp. 305-312. 

Fishes have been documented to respond with anti-predator behaviour to cues of both conspecifics as well as ecologically similar heterospecifics with which they co-occur (Chivers and Smith, 1998). The response to heterospecific alarm cues is innate in closely related species, and learned in distantly related species (Smith, 1982 Pollock et al., 2003). Prey warned by conspecific and heterospecific cues may have increased survival over prey that are not warned (Chivers et al., 2002). As well as increasing survival, heterospecific cues are also known to affect the timing of reproduction and the reproductive output of some species (Pollock et al., unpublished data). 

In this paper we review learned recognition of heterospecific alarm cues by prey fishes. We do this by providing a case study of the fathead minnow (Pimephales promelas)/bTOok stickleback Culaea inconstans) alarm systems. Fathead minnows and brook stickleback commonly occur together in a diversity of water bodies. They share a similar suite of predators and consequently cross-species responses to alarm cues should be highly advantageous. 

Pollock et al (2003) were the first to document the ability of minnows to learn to recognize heterospecific cues as an indication of predation. In their study a naturally occurring population of fathead minnows allopatric with brook stickleback did not respond to the skin extract of stickleback with an antipredator response. Stickleback fish were then introduced into the pond with the minnows and the two species were left to coexist for a period of five years. Following the period of co-existence, minnows were tested in the laboratory for a response to stickleback alarm cues. Not only did minnows now respond to stickleback cues, but they did so with the same intensity as they did to their own conspecific cues. A field experiment was also able to document a significant avoidance of stickleback skin extract in the wild. 

To be sure that individual learning and not rapid selection on the population accounted for the documented response. Pollock et al. (2003) collected minnow eggs from the pond and reared them in the laboratory. Once the fry had reached several months of age they were tested for a response to stickleback cues as well as to their own conspecific cues. Results indicated that while the fish responded to their own cues they failed to respond to stickleback cues. Taken together, these studies indicate that minnows are able to acquire the ability to respond to stickleback alarm cues, and that the response occurs through learning and is not an innate response. 

Chivers et al. (2002) tested whether or not learned responses could result in a survival benefit, besides confirming that fish could learn unknown heterospecific cues through the diet or a predator. In a two-part study, fathead minnows were exposed to chemical stimuli collected from rainbow trout (Oncorhynchus mykiss) fed a mixed diet of either minnows and brook stickleback, or swordtail and stickleback. To test if the minnows had acquired recognition of stickleback alarm cues, Chivers et al. (2003) exposed the fish to stickleback alarm cues and introduced an unknown predator, yellow perch or northern pike. Both perch and pike took longer to initiate an attack on minnows that were previously exposed to trout fed minnows and stickleback than those previously exposed to trout fed swordtails and stickleback. These results show again that fishes are able to learn novel cues through association with known cues in a predator s diet. Furthermore, it shows that anti-predator responses to these newly learned cues could result in a survival benefit. 

THE RESPONSE OF PREY FISHES TO CHEMICAL ALARM CUES WHAT RECENT FIELD EXPERIMENTS REVEAL ABOUT THE OLD... 

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