Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas

Young-of-the-year, predator-naive fathead minnows, Pimephales promelas , from a pikesympatric population did not respond to chemical stimuli from northern pike, Esox Indus , while wild-caught fish of the same age and size did. These results suggest that chemical predator recognition is a result of previous experience and not genetic factors, Wild young-of-the-year minnows responded to pike odour with a response intensity that was similar to that of older fish, demonstrating that the ability to recognize predators is learned within the first year. The intensity of response of wild minnows which had been maintained in a predator free environment for 1 year was similar to that of recently caught minnows of the same age, suggesting that reinforcement was not required for predator recognition to be retained. Naive minnows that were exposed simultaneously to chemical stimuli from pike (a neutral stimulus) and minnow alarm substance exhibited a fright response upon subsequent exposure to the pike stimulus alone. Predator-naive minnows exposed simultaneously to chemical stimuli from pike and glass-distilled water did not exhibit a fright response to the pike stimulus alone. These results demonstrate that fathead minnows can acquire predator recognition through releaserinduced recognition learning, thus confirming a known mechanism through which alarm substance may benefit the receivers of an alarm signal.     

Chemically mediated learning in juvenile rainbow trout. Does predator odour pH influence intensity and retention of acquired predator recognition?

The prediction that variability in ambient pH will influence the intensity and retention of learned predator recognition in juvenile rainbow trout Oncorhynchus mykiss was tested under laboratory conditions. Juvenile rainbow trout were conditioned to recognize the odour of a novel predator at pH 6·0 or 7·0 and then tested for learned recognition of the predator odour at pH 6·0 or 7·0 at 2 or 7 days post-conditioning. When tested 2 days post-conditioning, rainbow trout exhibited a significant learned antipredator response regardless of predator odour pH. The response was stronger, however, when the test pH matched the conditioning pH. When tested 7 days post-conditioning, rainbow trout only exhibited a learned response when conditioning and testing pH were the same. These results demonstrate that episodic acidification may impair the strength and retention of acquired predator recognition learning. Given the demonstrated survival benefits associated with learned predator recognition in prey fishes, such impairment will probably have considerable negative impacts at both individual and population levels.     

Vulnerability to predation and physiological stress responses of experimentally descaled juvenile chinook salmon,Oncorhynchus tshawytscha

Synopsis Juvenile salmonids,Oncorhynchus spp., commonly encounter conditions (e.g., during hatchery release and dam passage) that result in damage to the skin, scale, and slime complex. We conducted laboratory experiments to determine if descaling of juvenile chinook salmon,O. tshawytscha, increased their vulnerability to predation, and to assess the physiological stress responses elicited by descaling. Salmon were experimentally descaled on either 10% or 20% of their total body area. When offered equal numbers of control and descaled juvenile chinook salmon, northern squawfish,Ptychocheilus oregonensis, did not consume significantly more of either prey type (48–60% of consumed prey were descaled). Juvenile chinook salmon descaled on 10% of their body area did show significant physiological stress responses, however. Mean concentrations of plasma cortisol peaked 1 h after descaling, and returned to control levels by 12 h. Plasma glucose peaked 3 h post-treatment and remained elevated for 24 h. Plasma lactate increased immediately following treatment and returned to undisturbed control levels by 3 h. The osmoregulatory response of plasma potassium was highly variable, but plasma sodium decreased immediately and remained low for 24 h. The observed physiological responses suggest that descaling of juvenile chinook salmon could result in decreased resistance to disease and other stressors encountered in the field, possibly leading to reduced performance capacity and lowered survival.     

Population Differences in Responses of Fathead Minnows (Pimephales promelas) to Visual and Chemical Stimuli from Predators

Fathead minnows (Cyprinidae: Pimephales promelas) from a population that is sympatric with predatory northern pike (Esocidae: Esox lucius) exhibited a fright reaction to the visual stimulus of a live northern pike significantly more often than minnows from a population that is allopatric with pike. The fright response included increased use of shelter, dashing and freezing. Minnows from the pike-sympatric population also exhibited a significantly greater fright response, measured as a reduction in activity, following exposure to chemical stimuli from pike (i.e. water from a tank that had contained a pike) than did minnows from the pike-allopatric population. There was no significant change in activity by minnows from either population following exposure to chemical stimuli from nonpiscivorous peacock gudgeons (Eleotridae: Tateurndina ocellicauda), suggesting that the difference between the two populations is specific to stimuli from pike rather than a general difference in response to chemical stimuli from heterospecific fishes. Fathead minnows apparently utilize at least a two-tiered predator recognition system that incorporates both visual and chemical cues.     

Acquired Recognition of Predator Odour in the European Minnow (Phoxinus phoxinus)

Naive European minnows (Phoxinus phoxinus) do not show a fright reaction when they first encounter the odour of a natural predator (the pike: Esox lucius) or the odour of a non-piscivorous exotic (tilapia: Tilapia mariae). A conditioned fright response to both these odours will however develop if minnows experience them in a potentially dangerous situation, for example, in conjunction with Schreckstoff, the ostariophysian alarm pheromone. Although minnows respond to both odours the reaction to the tilapia odour is reduced. This suggests that a constraint on learning is involved. Olfactory recognition is particularly valuable for detecting predators that hunt in conditions where visibility is poor.     

Acquired Recognition of Chemical Stimuli from Pike,Esox lucius,by Brook Sticklebacks,Culaea inconstans (Osteichthyes,Gasterosteidae)

In this study we test whether brook sticklebacks (Culaea inconstans) can acquire predator recognition through releaser-induced recognition learning, i.e. simultaneous exposure to aversive ('releasing') stimuli and neutral stimuli causing learned aversion to the neutral stimuli. We exposed wild-caught pike-naive brook sticklebacks (collected from a creek containing fathead minnows, Pimephales promelas, but not pike, Esox lucius) to chemical stimuli from pike that were mixed with brook stickleback skin extract, fathead minnow skin extract, or a control of distilled water. In subsequent tests 2 d later, when only pike stimuli were presented, sticklebacks conditioned with stickleback skin extract and fathead minnow skin extract exhibited antipredator behaviour (i.e. increased schooling and movement toward the substrate), while those conditioned with distilled water did not. Sticklebacks conditioned with stickleback skin extract responded to pike with a more intense response, in terms of movement toward the substrate, than those conditioned with fathead minnow skin extract, suggesting that conspecific skin extract may be a stronger stimulus than heterospecific skin extract for learning recognition of predators. To our knowledge this is the first study to demonstrate that an acanthopterygian fish can acquire predator recognition through the pairing of conspecific alarm pheromone with the cue of a predator. Furthermore, our results are the first to demonstrate that fish can acquire predator recognition through the pairing of a heterospecific alarm pheromone with the cue of a predator. These results suggest that brook sticklebacks will benefit by being in close proximity to fathead minnows. Acquired predator recognition has long-term consequences in mediating predator-prey interactions.     

Ontogenetic variations in the type and size of prey consumed by juvenile coho,Oncorhynchus kisutch,and chinook,O. tshawytscha,salmon

Synopsis Stomach contents of juvenile coho,Oncorhynchus kisutch, and chinook,O. tshawytscha, salmon collected in purse seines off the coast of Washington and Oregon were examined for variations related to predator size. There was a general trend toward increasing consumption of fish with increasing body size, due mainly to the increase in northern anchovy biomass consumed by the larger salmon. Most of the major prey taxa showed significant differences among the size classes examined for both salmon species. There was a direct relationship between predator and prey size for both coho and chinook, but considerable variation was found in prey length consumed within each size class. Prey width did not provide as good a fit as prey length for either species. In general, coho consumed larger fish prey in relation to their body length than chinook but there were substantial differences by month or year of collection.     

Wild chinook salmon survive better than hatchery salmon in a period of poor production

The population dynamics of chinook salmon (Oncorhynchus tshawytscha) from the Cowichan River on Vancouver Island, British Columbia, Canada are used by the Pacific Salmon Commission as an index of the general state of chinook salmon coast wide. In recent years the production declined to very low levels despite the use of a hatchery that was intended to increase production by improving the number of smolts entering the ocean. In 2008, we carried out an extensive study of the early marine survival of the hatchery and wild juvenile chinook salmon. We found that both rearing types mostly remained within the Gulf Islands study area during the period when most of the marine mortality occurred for the hatchery fish. By mid September, approximately 1.3% of all hatchery fish survived, compared to 7.8%–31.5% for wild fish. This six to 24 times difference in survival could negate an estimated increased egg-to-smolt survival of about 13% that is theorized to result through the use of a hatchery. Estimates of the early marine survival are approximate, but sufficient to show a dramatic difference in the response of the two rearing types to the marine nursery area. If the declining trend in production continues for both rearing types, modifications to the hatchery program are needed to improve survival or an emphasis on improving the abundances of wild stocks is necessary, or both. The discovery that the juvenile Cowichan River chinook salmon remain within a relatively confined area of the Gulf Islands within the Strait of Georgia offers an excellent opportunity to research the mechanisms that cause the early marine mortalities and hopefully contribute to a management that improves the production.     

Background Predation Risk and Learned Predator Recognition in Convict Cichlids: Does Risk Allocation Constrain Learning?

Exposure to elevated levels of background predation risk is known to shape the behavioural response of prey organisms to known and unknown predation threats. However, less is known regarding the effects of background predation risk on predator recognition learning. Here, we test the potential effects of elevated background predation risk on the strength and retention of learned predator recognition in juvenile convict cichlids (Amatitlania nigrofasciata). In a series of laboratory trials, we exposed shoals of juvenile cichlids to conditions of elevated (vs. low) levels of background risk and then conditioned them to recognize a novel predator odour (rainbow trout, Oncorhynchus mykiss). The results of our first experiment demonstrate that despite showing reduced response intensities during initial conditioning (due to risk allocation), conditioned cichlids from high vs. low background risk show similar intensities of learned recognition when tested 24 h post‐conditioning. Moreover, elevated levels of background risk induced a predator avoidance response among unconditioned cichlids (due to induced neophobia). Our second experiment demonstrates that while we find no difference in the strength of learning when tested 24 h post‐conditioning, retention of acquired recognition is enhanced among cichlids from the high background predation risk treatment. Together, our results highlight the complex interacting effects past experience plays in shaping the response to acute predation threats.     

Behavioural responses of naive Arctic charr young to chemical cues from salmonid and non-salmonid fish

The ability to distinguish among chemical cues from multiple predators is of key adaptive value for many prey fish. We examined the attractiveness and repulsiveness of chemical stimuli from different coexisting fish species fed on different diets on the behaviour of hatchery reared Arctic charr young in a Y-maze fluviarum, where the charr could choose between two sides either with control water or stimulus water with fish odour. We used stimuli from (1) matching sized conspecifics, large (2) Arctic charr, (3) salmon, (4) brown trout and (5) brown trout fed on Arctic charr fry. Other salmonids were given pellet food. Additional fish odour treatments included piscivorous (6) pike and (7) burbot. In the control trials both sides received control water. Arctic charr young were expected to respond adaptively to the stimuli from coexisting piscivorous fish. The charr most strongly preferred water with the odour of their matching sized conspecifics, which was the only fish odour they were familiar with before the experiments. They also showed significant preference for other salmonid odours, even though these fish are potential predators on small charr. Chemical stimuli from pike and burbot, on the contrary, were strongly avoided, and burbot odour even prevented the charr to swim and enter the lateral halves of the fluviarum. Moreover, odour from brown trout fed on Arctic charr fry was avoided when compared to stimuli from trout fed on pellets. Although the Arctic charr young were completely naive regarding piscivores, the fact that they could distinguish between different predator taxa and diets on the basis of chemical cues only reflects the long coevolutionary history of these fish populations.     

Predation on the Invasive Copepod,Pseudodiaptomus forbesi,and Native Zooplankton in the Lower Columbia River: An Experimental Approach to Quantify Differences in Prey-Specific Feeding Rates

Invasive planktonic crustaceans have become a prominent feature of aquatic communities worldwide, yet their effects on food webs are not well known. The Asian calanoid copepod, Pseudodiaptomus forbesi, introduced to the Columbia River Estuary approximately 15 years ago, now dominates the late-summer zooplankton community, but its use by native aquatic predators is unknown. We investigated whether three species of planktivorous fishes (chinook salmon, three-spined stickleback, and northern pikeminnow) and one species of mysid exhibited higher feeding rates on native copepods and cladocerans relative to P. forbesi by conducting `single-prey’ feeding experiments and, additionally, examined selectivity for prey types with `two-prey’ feeding experiments. In single-prey experiments individual predator species showed no difference in feeding rates on native cyclopoid copepods (Cyclopidae spp.) relative to invasive P. forbesi, though wild-collected predators exhibited higher feeding rates on cyclopoids when considered in aggregate. In two-prey experiments, chinook salmon and northern pikeminnow both strongly selected native cladocerans (Daphnia retrocurva) over P. forbesi, and moreover, northern pikeminnow selected native Cyclopidae spp. over P. forbesi. On the other hand, in two-prey experiments, chinook salmon, three-spined stickleback and mysids were non- selective with respect to feeding on native cyclopoid copepods versus P. forbesi. Our results indicate that all four native predators in the Columbia River Estuary can consume the invasive copepod, P. forbesi, but that some predators select for native zooplankton over P. forbesi, most likely due to one (or both) of two possible underlying casual mechanisms: 1) differential taxon-specific prey motility and escape responses (calanoids > cyclopoids > daphnids) or 2) the invasive status of the zooplankton prey resulting in naivety, and thus lower feeding rates, of native predators feeding on invasive prey.     

Predator recognition learning in rainbow darters Etheostoma caeruleum: specific learning and neophobia

This study investigated whether rainbow darters Etheostoma caeruleum can learn to recognize unfamiliar predators through the process of classical conditioning. Etheostoma caeruleum were conditioned by exposing them simultaneously to their chemical alarm cues (a known fright stimulus) and either chemical cues from larval ringed salamanders Ambystoma annulatum (unfamiliar predator) or to a blank water cue (control). Conditioning could result in either specific learning of the A. annulatum cue or increased wariness in response to any novel cue (neophobia). To distinguish between these possibilities, E. caeruleum in both groups were exposed to either A. annulatum cues alone or to chemical cues from western rat snakes Pantherophis obsoletus (novel cue) 2 days after conditioning. Treatment (A. annulatum‐conditioned) E. caeruleum, but not control E. caeruleum, showed a fright response when they were exposed to both the conditioned (A. annulatum) and novel (P. obsoletus) cues, indicating increased sensitivity to new stimuli. When E. caeruleum were retested after an additional 32 days, however, the fright response occurred only following exposure to the conditioned (A. annulatum) stimulus, indicating that specific learning of the A. annulatum cue had been retained whereas the neophobia to novel stimuli was temporary.     

Innate predator recognition and fright response in related populations of Oncorhynchus mykiss under different predation pressure

Innate predator recognition and fright response behaviours were compared in a laboratory study between second generation offspring from two related populations of steelhead trout Oncorhynchus mykiss from Sashin Creek, Alaska. The stream population was anadromous and co-occurred with Dolly Varden Salvelinus malma , a piscivore and salmonid predator. Sashin Lake, formerly fishless, was stocked with fish from the stream population in 1926 and that population has been isolated from heterospecific piscine predation ever since. Fish from the lake population were predicted to show diminished innate fright response to Dolly Varden scent relative to the stream population. The behaviour of 60 individual juvenile O. mykiss from each population was measured and observed in aquaria before and after exposure to chemical cues of Dolly Varden, conspecific skin extract, or a control of distilled water. The alarm substances caused significant behavioural changes in both populations in the amount of time spent motionless, time spent in the lower water column and feeding frequency. No significant differences were observed between the stream and lake populations in the change in behaviour between pre- and post-stimulus observation periods for any of the measured fright responses, indicating that the sequestered lake population has not lost the ability to detect or respond to conspecific alarm substances or Dolly Varden scent.     

棉铃虫成虫对两种关键花香气味的联系性学习

为了明确棉铃虫对苯乙醛和乙酸苯甲酯两种关键花香气味的联系性学习行为,在室内分别测定了不同学习训练的棉铃虫雌雄成虫对两种关键花香气味的选择偏好性反应和雄成虫的触角电位反应。偏好性测定结果表明,无花香气味接触经历的棉铃虫对苯乙醛和乙酸苯甲酯的选择频次均无显著差异,且单纯的花香气味接触经历也不能诱导棉铃虫气味偏好性的显著改变,唯有花香气味接触经历伴随蔗糖溶液进行强化训练时,才能诱导气味偏好性的显著性改变。从对两种花香气味的联系性学习看,棉铃虫更容易将苯乙醛与蔗糖溶液进行联系性学习,而不容易将乙酸苯甲酯与蔗糖溶液进行联系性学习。从性别差异看,雌虫比雄虫具有更强的将花香气味与蔗糖溶液进行联系性学习的能力。触角电位测定结果表明,不同学习训练的棉铃虫雄成虫对两种花香气味和绿叶气味顺-3-己烯-1-醇的EAG反应值之间不存在显著性差异。总之,花香气味伴随食物资源的联系性学习经历,能够明显提高棉铃虫成虫对花香气味的选择偏好,可以此为基础进一步优化花香引诱剂的配方设计和应用技术。     

Improving anti‐predator responses of hatchery reared salmonids by social learning

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been ‘trained’ by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Factors affecting the recognition of population-specific odours by juvenile coho salmon*

Juvenile coho salmon Oncorhynchus kisutch from the Quinsam, Big Qualicum and Puntledge Rivers, British Columbia, Canada, discriminated between the chemical emanations of similarly aged salmon from their own and another population. However, common rearing during the embryonic, larval and early free-swimming stages rendered families more attractive to each other than they were otherwise. Preference among populations was also influenced by quantity of odour produced by the fish. Some fish, notably the Quinsam River population, appeared to produce greater quantities of attractants than other fish. Finally, the salmon also preferred water conditioned by faeces of members of their own population over blank water and, in one of two experiments, over water conditioned by faeces of non-population members, suggesting that at least some of the odourants mediating intraspecific discriminations are present in faeces. These results confirm earlier studies demonstrating that salmonid populations differ in odours distinguishable by conspecifics but indicate that experiments investigating this phenomenon must be designed carefully to avoid bias owing to differences other than population-specific traits. The role of population recognition in the lives of salmonids is unclear; it might be a manifestation of more general imprinting for homing, of sibling recognition, or it might play a role in mate choice.     

Learned Recognition of Novel Predator Odour by Zebra Danios, Danio Rerio, Following Time-shifted Presentation of Alarm Cue And Predator Odour

Fishes in the superorder ostariophysi possess specialized epidermal cells that contain an alarm cue. Fish associate novel odours, such as the odour of a predator, with predation risk after a single, simultaneous exposure to the novel odour and alarm cue. Thereafter, the novel cue is recognized as an indicator of risk and its presence induces antipredator behaviour. Two common antipredator behaviours are reduction in activity and movement to the bottom. This phenomenon has been demonstrated many times in the laboratory setting for a variety of aquatic taxa. In nature however, the detection of novel predator odour may be time-shifted with respect to the detection of alarm cues. Is there a critical period immediately upon the detection of alarm cue in which associative learning can occur? We presented zebra danios, Danio rerio, with the odour of northern pike, Esox lucius, 5?min after presenting them with either alarm cue or water (control). During a predation event, 5?min is a long time. When later retested with pike odour alone, zebra fish conditioned with alarm cue significantly increased antipredator behaviour in terms of decreased activity and movement towards the bottom. Control fish did not recognize pike odour as dangerous when retested. These data show that learned recognition of predation risk is sufficiently robust to accommodate ecologically realistic temporal shifts in stimulus presentation.     

Bitterling as models for studies of sperm competition

The plight of the world fish stocks is all too well documented. As part of an ongoing attempt to bolster fish stocks for both commercial and conservation purposes, many fish are reared in captivity and released into the wild. It is well known that hatchery‐reared fish have low post‐release survival compared with wild fish of similar age. Part of the reason for this high mortality is that hatchery fish show deficits in virtually all aspects of their behaviour, including prey selection and predator avoidance. Much behaviour requires repeated experience so that it may become fine‐tuned to prevailing circumstances via learning during development. It has been suggested that inappropriate behaviour is encouraged when fish are reared in the unnatural surroundings of the hatchery. However, hatchery fish can be taught to recognise live, novel prey items and predators and the rate of learning is increased in the presence of a more knowledgeable conspecifics. Here we present data showing how social learning protocols can be used to dramatically increase foraging success in juvenile Atlantic salmon. We also outline related aspects of our ongoing research and discuss some of the possibilities for altering hatchery practices to maximize post‐release survival.     

Effects of spatial scale and foraging efficiency on the predictions made by spatially-explicit models of fish growth rate potential

Synopsis Spatially-explicit modeling of fish growth rate potential is a relatively new approach that uses physical and biological properties of aquatic habitats to map spatial patterns of fish growth rate potential. Recent applications of spatially-explicit models have used an arbitrary spatial scale and have assumed a fixed foraging efficiency. We evaluated the effects of spatial scale, predator foraging efficiency (combined probabilities of prey recognition, attack, capture, and ingestion), and predator spatial distribution on estimates of mean growth rate potential of chinook salmon,Oncorhynchus tshawytscha. We used actual data on prey densities and water temperatures taken from Lake Ontario during the summer, as well as, simulated data assuming binomial distribution of prey. Results show that a predator can compensate for low foraging efficiency by inhabiting the most profitable environments (regions of high growth rate potential). Differences exist in predictions of growth rate potential across spatial scales of observation and a single scale may not be adequate for interpreting model results across seasons. Continued refinements of this modeling approach must focus on the assumptions of stationary distributions of predator and prey populations and predator foraging tactics.