Coral degradation alters predator odour signatures and influences prey learning and survival.

Habitat degradation is a key factor leading to the global loss of biodiversity. This problem is particularly acute in coral reef ecosystems. We investigated whether recognition of predator odours by damselfish was influenced by coral degradation and whether these changes altered survival in the wild. We taught whitespot damselfish to recognize the odour of a predator in the presence of live/healthy coral or dead/degraded coral. Fish were tested for a response to predator odours in environments that matched their conditioning environment or in environments that were mismatched. Next, we taught blue damselfish to recognize the odour of three common reef predators in live and degraded coral environments and then stocked them onto live or degraded patch reefs, where we monitored their subsequent response to predator odour along with their survival. Damselfish learned to recognize predator odours in both coral environments, but the intensity of their antipredator response was much greater when the conditioning and test environments matched. Fish released on degraded coral had about 50% higher survival if they had been trained in the presence of degraded coral rather than live coral. Altering the intensity of antipredator responses could have rather profound consequences on population growth.

Social learning of predators in the dark: understanding the role of visual, chemical and mechanical information.

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.

Do fathead minnows, Pimephales promelas Rafinesque, alter their club cell investment in responses to variable risk of infection from Saprolegnia?

Fish in the Superorder Ostariophysi possess large epidermal club cells that release chemical cues warning nearby conspecifics of danger. Despite the long-held assumption that such club cells evolved under the selective force of predation, recent studies demonstrated that predation has no effect on club cell investment. Rather, club cells have an immune function and cell production may be stimulated by skin-penetrating pathogens and parasites. The current work investigates whether fathead minnows, Pimephales promelas, alter their club cell characteristics based on variation in infection risk. In a 2 × 3 design, we exposed minnows to infective cysts of two oomycete species (Saprolegnia ferax and S. parasitica) at three different concentrations (2, 20 or 200 cysts L(-1)). Club cell characteristics (number and size) were quantified 12 days after exposure. Saprolegnia parasitica is thought to be more pathogenic than S. ferax, hence we predicted greater club cell investment and a larger turnover rate of cells by minnows exposed to S. parasitica than S. ferax. We also predicted that minnows exposed to higher numbers of cysts should invest more in club cells and have a higher turnover rate of cells. We found no difference in club cell density or size between fish exposed to the two Saprolegnia species; however, fish exposed to high concentrations of pathogens had smaller club cells than those exposed to low concentrations, indicating a higher rate of turnover of cells in the epidermis.

Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout Oncorhynchus mykiss.

The effects of food ration and social context, as well as possible interactions, on the antipredator behaviour of juvenile rainbow trout Onchorhynchus mykiss were investigated in a pair of laboratory studies. In experiment 1, pairs of dominant and subordinate O. mykiss were exposed to conspecific alarm cues when maintained under high or low food rations. Under high food rations, dominant individuals responded to predation risk, whereas subordinates used the opportunity to feed. Under low food ration, however, the opposite pattern was observed, where subordinates responded to predation cues and dominants did not. Experiment 2 consisted of performing the same experiment, however separating the dominant and subordinate O. mykiss 3 h before testing. When tested separately, dominant and subordinate individuals did not differ in their responses to alarm cues, regardless of food ration. These results demonstrate that there is a complex interaction between current energy status and social context on decision making by prey animals.

Massive mortality of common carp (Cyprinus carpio carpio) in the St. Lawrence River in 2001: diagnostic investigation and experimental induction of lymphocytic encephalitis.

A massive fish kill affecting exclusively common carp (Cyprinus carpio carpio) in the St. Lawrence River, Québec, Canada, during the summer of 2001 was investigated by use of laboratory diagnostic methods and by an attempt to experimentally induce the disease. The ultimate causes of mortality were opportunistic bacterial infections with Aeromonas hydrophila and Flavobacterium sp. secondary to immunosuppression induced by physiologic (i.e., spawning) and environmental (i.e., high temperatures and low water levels) stressors, and possibly enhanced by an infection causing lymphocytic encephalitis observed in 9 of 18 (50%) fish examined. Experimental induction of disease was attempted in captured wild carp by administration of crude and filtered (particulate <0.22 microm) inocula prepared from a homogenate of tissues from carp affected by the natural outbreak. Although significant clinical disease or mortality was not induced by experimental challenge, lymphocytic encephalitis similar to the one observed in naturally affected carp was induced in four of seven (57%) fish administered crude inoculum and four of seven (57%) fish administered filtered inoculum. None of the control fish inoculated with sterile phosphate-buffered saline (n = 6) were affected by encephalitis. The cause of the encephalitis observed in carp from the natural outbreak and in experimentally inoculated fish could not be determined by use of virus isolation and transmission electron microscopy.

Intra- and interspecific avoidance of areas marked with skin extract from brook sticklebacks (Culaea inconstans) in a natural habitat.

The detection of a chemical alarm pheromone may allow receivers to avoid areas where a predator has captured the prey's conspecifics. We marked minnow traps with either brook stickleback (Culaea inconstans) skin extract or a control of distilled water and tested whether sticklebacks avoided the skin extract marked traps in a natural habitat. Significantly more sticklebacks were captured in traps marked with control water, thereby demonstrating avoidance of conspecific skin extract. The stickleback captured in traps marked with conspecific extract were significantly smaller than those captured in traps marked with control water, implicating ontogenetic factors (i.e., experience or physiological development) in the development of the response. We also captured significantly fewer finescale dace (Chrosomus neogaeus) and fathead minnows (Pimephales promelas) in traps marked with skin extract. These data suggest that dace and minnows may benefit by avoiding areas where predators have recently captured sticklebacks.

The role of olfaction in chemosensory-based predator recognition in the fathead minnow,Pimephales promelas.

Solitary fathead minnows (Pimephales promelas) were rendered anosmic and exposed to chemical stimuli from a predatory northern pike (Esox lucius) to determine the role of olfaction in the minnow's ability to recognize predators on the basis of chemical stimuli. Anosmic fish did not respond to the pike stimuli with a typical fright reaction, while control fish, with intact olfactory receptors, did. These results demonstrate that the olfactory system is necessary for the ability of fathead minnows to recognize northern pike as a predator and that the gustatory and single-celled chemosensory systems are not sufficient for this recognition in the absence of olfactory input. Olfactory impairment was behaviorally confirmed by exposing minnows to alarm substance (Schreckstoff).

Are chemical alarm cues conserved within salmonid fishes?

A wide diversity of fishes possess chemical alarm signalling systems. However, it is not known whether the specific chemicals that act as alarm signals are conserved within most taxonomic groups. In this study we tested whether cross-species responses to chemical alarm signals occurred within salmonid fishes. In separate laboratory experiments, we exposed brook charr (Salvelinus fontinalis), brown trout (Salmo trutta), and rainbow trout (Oncorhynchus mykiss) to chemical alarm signals from each of the three salmonid species and from swordtails (Xiphophorus helleri). In each case, the test species responded with appropriate antipredator behavior to all three salmonids alarm cues, but did not react to swordtail cues. These data suggest that chemical alarm cues are partially conserved within the Family Salmonidae. For each species tested, the intensity of the response was stronger to conspecific alarm cues, than to heterospecific alarm cues, indicating that salmonids could distinguish between chemical cues of conspecifics versus heterospecifics. These results suggest that the chemical(s) that act as the alarm cues may be: 1) identical and that there may be other chemical(s) that allow the test fish to distinguish between conspecifics and heterospecifics, or 2) that the cues that act as signals are not identical, but are similar enough to be recognized.

Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators.

We examined the effects of predator diet on the antipredator responses of larval woodfrogs (Rana sylvatica). We found that tadpoles showed stronger responses to fish (Perca flavescens) that were fed tadpoles than those fed invertebrates. Similarly, we found that tadpoles responded more strongly to larval dragonflies (Anax spp.) fed tadpoles than to dragonflies fed invertebrates. The overall intensity of response of tadpoles to fish was much stronger than that to dragonflies. Predator diet effects are not ubiquitous in predator-prey systems. We discuss possible reasons why predator diet effects are seen in some, but not all, predator-prey systems.

Early warning in the predation sequence: A disturbance pheromone in Iowa darters (Etheostoma exile).

The probability of prey avoiding a predator's attack should increase if the predator's presence is detected at an early stage in the predation sequence. In this study, we tested whether threatened Iowa darters (Etheostoma exile) release disturbance pheromones that warn conspecifics of the presence of predation threat. Pairs of aquaria were visually isolated from one another, but connected chemically by water circulating between them. Darters in one aquarium were observed before and after darters in the other aquarium were chased with a model predator. In control tests, the model was moved in the same manner but there were no darters in the upstream tank. Darters receiving water from threatened fish increased vigilance behavior and decreased movement. Vigilant fish raised their head above the substratum, propping themselves up on their pectoral fins and/or arching their neck dorsally, pointing the snout upward. Exposure to water from disturbed darters suppressed exploratory behavior and resulted in movement by short rapid hops that ended abruptly in a rigid, alert posture. This study suggests that Iowa darters release a disturbance pheromone that can provide conspecifics with an early warning of predation risk.

Risk-sensitive habitat use by brook stickleback (Culaea inconstans) in areas associated with minnow alarm pheromone.

Brook stickleback (Culaea inconstans) share habitat and predators with cyprinid species, and they exploit the alarm pheromone of fathead minnows (Pimephales promelas) to avoid areas of high predation risk. In this field experiment, we measured the retention and duration of area avoidance by brook stickleback from areas marked with alarm pheromone of fathead minnows. Area avoidance was greatest during the first 2 hr after the source of the alarm pheromone was removed (P<0.05), but after 4 hr, area use was not significantly different from premarking levels. This study shows that brook stickleback: (1) use the alarm pheromone of fathead minnows to avoid high risk areas, (2) continue to avoid locations associated with predation risk after the source of the pheromone has gone, and (3) avoid risky areas temporarily, and resume use of risky areas after 2-4 hr. This behavioral response by stickleback to minnow alarm pheromone could serve to minimize risk of predation.

Effects of diet on localized defecation by Northern Pike,Esox lucius.

Fathead minnows (Pimephales promelas) are able to detect conspecific alarm pheromone in the feces of northern pike (Esox lucius) and have been shown to avoid areas labeled with the feces of pike that were fed minnows. The minnows did not avoid areas labeled with the feces of pike that were fed swordtails (Xiphophorous helleri), which lack ostariophysan alarm pheromone. In laboratory experiments, pike fed a diet of minnows localized their defecation away from their foraging area. It has been suggested that in doing so, pike may remove chemical cues that label their foraging area as dangerous to prey species. As yet there has been no conclusive evidence to support this hypothesis. In this experiment, we test the effects of different predator diets on localized defecation by pike. Pike were fed minnows, swordtails, or mice (Mus musculus). Swordtails and mice lack ostariophysan alarm pheromones. Area use and location of feces were recorded. Pike fed minnows spent significantly more time in the home area (i.e., area of the test tank where they were fed) and defecated significantly more often in the opposite end of the tank. Pike fed swordtails also exhibited a significant preference for the home area in area use, while those fed mice showed no such preference. When fed either swordtails or mice, there was no significant difference between the proportion of time spent and proportion of feces in each area of the test tank. These data suggest that pike localize their defecation only when consuming prey items containing alarm pheromone. The current findings support the hypothesis that pike localize their defecation to remove chemical cues from the foraging area of the home range in order to avoid chemically labeling their foraging area as dangerous to prey.

Brook charr alevins alter timing of nest emergence in response to chemical cues from fish predators.

Brook charr (Salvelinus fontinalis) lay their eggs in gravel nests called redds. The nests are not defended for extended periods and the eggs and young may be subject to predation from predators that travel through the substrate into the redd. In this study we tested whether long-term exposure of brook charr eggs to chemical cues from predatory sculpins (Cottus cognatus) resulted in an adaptive shift in the timing of emergence of charr alevins from artificial redds. We reared brook charr eggs in the presence of chemical cues from sculpins fed brook charr eggs, sculpins fed brine shrimp, and a well water control. Significantly more alevins emerged during the first week of the emergence period when exposed to chemical cues from sculpins fed eggs than from cues from sculpins fed brine shrimp or from well water. Alevins that emerged sooner were smaller and possessed larger yolk sacs than alevins that emerged later in the emergence period. Our results suggest that alevins that emerge sooner may escape predation in the redd, but may pay a cost in being under-developed upon emergence into the open water of the stream or lake.

Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): responses to alarm, disturbance, and predator cues.

Slimy sculpins (Cottus cognatus) are small benthic fish that commonly co-occur with predatory fishes throughout most of their range in North America. In two laboratory experiments we examined the nature and extent of responses of slimy sculpins to chemosensory cues from predatory brook trout (Salvelinus fontinalis) and chemical alarm cues released by conspecific sculpins. Sculpins responded to three different classes of chemical stimuli: (1) cues of predatory brook trout, (2) damage-released alarm cues from conspecific sculpins, and (3) disturbance cues from conspecific sculpins. Sculpins did not distinguish between trout fed different diets; however, the presence of damage-released alarm cues did enhance the intensity of response to the predator chemicals. A histological analysis of the skin of sculpins revealed the presence of large sacciform cells that may act as the source of chemical alarm signals.

Population and sex differences in antipredator responses of breeding fathead minnows (Pimephales promelas) to chemical stimuli from garter snakes (Thamnophis radix andT. sirtalis).

We conducted a predator bite survey on a population of fathead minnows (Pimephales promelas) considered to be under substantial predation pressure by western plains garter snakes (Thamnophis radix). Scarring, due to failed predation attempts by garter snakes and crayfish (Orconectes virilis), was observed significantly more often in breeding males than in breeding females and nonbreeding minnows. Likely, territorial nest defense under the edges of rocks along the water's edge, a habitat occupied by crayfish and frequented by snakes, caused the breeding males to be differentially vulnerable to predation. Under controlled laboratory conditions, breeding males from this population exhibited an antipredator response to chemical stimuli from live snakes (T. sirtalis andT. radix) significantly more often than breeding female minnows from the same population and breeding minnows of both sexes from a population that was presumed to be under lower predation pressure from snakes.

Ambient UV-B radiation causes deformities in amphibian embryos.

There has been a great deal of recent attention on the suspected increase in amphibian deformities. However, most reports of amphibian deformities have been anecdotal, and no experiments in the field under natural conditions have been performed to investigate this phenomenon. Under laboratory conditions, a variety of agents can induce deformities in amphibians. We investigated one of these agents, UV-B radiation, in field experiments, as a cause for amphibian deformities. We monitored hatching success and development in long-toed salamanders under UV-B shields and in regimes that allowed UV-B radiation. Embryos under UV-B shields had a significantly higher hatching rate and fewer deformities, and developed more quickly than those exposed to UV-B. Deformities may contribute directly to embryo mortality, and they may affect an individual's subsequent survival after hatching.

Avoidance response of juvenile Pacific treefrogs to chemical cues of introduced predatory bullfrogs.

Bullfrogs (Rana catesbeiana), native to eastern North America, were introduced into Oregon in the 1930's. Bullfrogs are highly efficient predators that are known to eat a variety of prey including other amphibians. In laboratory experiments, we investigated whether juvenile Pacific treefrogs (Hyla regilla) recognize adult bullfrogs as a predatory threat. The ability of prey animals to acquire recognition of an introduced predator has important implications for survival of the prey. We found that treefrogs from a population that co-occurred with bullfrogs showed a strong avoidance of chemical cues of bullfrogs. In contrast, treefrogs from a population that did not co-occur with bullfrogs, did not respond to the bullfrog cues. Additional experiments showed that both populations of treefrogs use chemical cues to mediate predation risk. Treefrogs from both populations avoided chemical alarm cues from injured conspecifics.

Avoidance response of a terrestrial salamander (Ambystoma macrodactylum) to chemical alarm cues.

Organisms from a wide variety of taxonomic groups possess chemical alarm cues that are important in mediating predator avoidance. However, little is known about the presence of such alarm cues in most amphibians, and in particular terrestrial salamanders. In this study we tested whether adult long-toed salamanders (Ambystoma macrodactylum) showed an avoidance response to stimuli from injured conspecifics. Avoidance of stimuli from injured conspecifics could represent avoidance of a chemical alarm cue or, alternatively, avoidance of a territorial pheromone or conspecific predator odor. Consequently, we also tested whether salamanders avoided stimuli from noninjured conspecifics. Salamanders avoided stimuli from injured but not from noninjured conspecifics. Therefore, we concluded that the response to injured conspecifics represents avoidance of a chemical alarm cue and not avoidance of a territorial pheromone or predator cue. This is the first clear demonstration of chemical alarm signaling by a terrestrial amphibian and the first report of chemical alarm signaling in an ambystomatid salamander. By avoiding an area containing stimuli from injured conspecifics, long-toed salamanders may lower their risk of predation by avoiding areas where predators are foraging.