Genetic control of predator avoidance behaviour in Daphnia

1. The vertical migration behaviour in electrophoretically distinguishable clones of Daphnia magna Straus was investigated. 2. Clones differed significantly in their tendency to stay near the surface of the tank during the light phase of the daily light/dark cycle, indicating that vertical migration has a genetic component. 3. There was a significant difference in behaviour between juvenile and adult Daphnia: overall the juveniles stayed closer to the water surface than the adults, but the characteristic pattern of clonal differences persisted in the juveniles. 4. When an adult population of each clone was exposed to a fish predator in an experimental tank, the position a clone maintained in the tank at the start of the day had a direct effect on its survival. Clones remaining near to the surface of the water suffered greatest predarion.     

Predator‐avoidance behaviour in a nocturnal petrel exposed to a novel predator

Many species of bird recognize acoustic and visual cues given by their predators and have complex defence adaptations to reduce predation risk. Recognition of threats posed by specific predators and specialized anti‐predation behaviours are common. In this study we investigated predator recognition and anti‐predation behaviours in a pelagic seabird, Leach's Storm‐petrel Oceanodroma leucorhoa, at a site where predation risk from Great Skuas Stercorarius skua is exceptionally high. Leach's Storm‐petrels breed in burrows and come on land only at night. Counter‐predator adaptations were investigated correlatively in relation to changing natural light levels at night, and experimentally in relation to nocturnal visual and acoustic signals from Great Skuas. Colony attendance by Leach's Storm‐petrels was attuned to changes in light conditions at night and was highest when nights were darkest. This behaviour is likely to reduce predation risk on land; however, specific recognition of Great Skuas and specialized defence behaviours were not found. Leach's Storm‐petrels, in particular apparently non‐breeding individuals, were entirely naïve to the threat posed by Great Skuas and were captured easily in a variety of different ways, on the ground and in the air. Lack of specialized behavioural adaptations in Leach's Storm‐petrels against Great Skuas may be because spatial overlap of breeding distributions of these species appears to be a rare and recent phenomenon.     

Group transmission of predator avoidance behaviour in a marine insect: The trafalgar effect

The approach of a predator model induces rapid changes in the locomotory behaviour of individuals at the periphery of flotillas of a marine insect, the ocean skater Halobates robustus Barber. There is an abrupt and substantial increase in velocity, frequency of turning, the number of apparently random encounters between individuals and also the frequency of changes in light reflection from the body surfaces. These behavioural responses are postulated to cause predator confusion and, less frequently, to initiate rapid, synchronous dispersal of the flotillas. Interactions between individuals in the flotillas mediate a rapid transmission of avoidance behaviour through the flotilla which, in our field experiments, greatly exceeded the speed of approach of a predator model. This behaviour (named the Trafalgar Effect) enables individuals to initiate avoidance behaviour before the approaching predator can be seen.     

Foraging strategy and predator avoidance behaviour: an intraspecific approach

Relationships between predator avoidance behaviour (scanning and flocking) and foraging were studied in Calidris alpina, to test predictions regarding the effect of foraging techniques on such behaviours. The scanning hypothesis predicts that individuals with a tactile hunting technique and individuals with a visual hunting technique (both continuous searchers) do not differ in any variable related to scanning behaviour. The flocking hypothesis predicts that visually hunting individuals witl tend to form smaller flocks than tactile-foraging individuals. The two continuous feeding strategies did not differ among individuals in vigilance rate, nor in vigilance time or mean scan duration. However, with respect to flocking behaviour, visual foragers differed from tactile foragers in foraging flock size. The relationships between flocking behaviour and foraging strategy are discussed. The pattern found at the intraspecific level are the same as those found at interspecific level.     

Chemically induced predator avoidance behaviour in the burrowing bivalve Macoma balthica

The responses of the burrowing bivalves Macoma balthica and Cerastoderma edule to chemical cues emitted by feeding shore crabs Carcinus maenas were investigated. M. balthica held in the laboratory and exposed to chemical signals in effluent water discharging from tanks containing C. maenas fed 20 M. balthica day^− 1 reacted by increasing their burial depths from approximately 30 mm to depths of > 60 mm, over a period of several days. When the signal was removed the bivalves gradually returned to their original depth over 5 days. C. edule similarly exposed to effluent from crabs feeding on conspecifics showed no response. In an attempt to identify the signal inducing this burrowing response, M. balthica were exposed to a variety of chemical signals. Crabs fed M. balthica elicited the strongest response, followed by crabs fed C. edule. There were also small responses to effluent from crabs fed on fish, crabs previously fed on M. balthica and to crab faeces, but no responses to starved crabs, crushed M. balthica, or controls. We conclude that increased burrowing depth of M. balthica is induced by some as yet unidentified chemical cue produced by feeding crabs and is strongest when the crabs were fed on M. balthica. Unexpectedly, neither the presence of crabs themselves, nor of damaged conspecifics, was effective in eliciting a burrowing response. The mortality rates of M. balthica and C. edule selected by crabs when burrowed at normal depths and after exposure to effluent from feeding crabs were different. Crabs selected 1.5 times more C. edule than M. balthica when both species were burrowed at their normal depths, but 15 times more after the tanks had been exposed to effluent from feeding crabs for 5 days. The burrowing response of M. balthica thus appears to reduce mortality significantly by displacing predation pressure on to the more accessible C. edule.     

Influence of rearing and experimental temperatures on predator avoidance behaviour in a freshwater pulmonate snail

1. Predicted increases in the temperature of freshwaters is likely to affect how prey species respond to predators. We investigated how the predator avoidance behaviour of the freshwater pulmonate snail Lymnaea stagnalis is influenced by the temperature at which it was reared and that at which behavioural trials were carried out. 2. Crawl‐out behaviour of juvenile snails from two populations (high predation risk versus low predation risk) reared at either 15 or 20 °C was assessed in response to predation cues (predatory fish kairomones and conspecific alarm cues) in behavioural trials at both 15 and 20 °C. 3. Trial temperature had a significant effect on the time that snails spent in avoidance, regardless of their population of origin. Crawl‐out behaviour was greater during behavioural trials at 15 °C, but there was no effect of trial temperature on the speed with which animals showed avoidance behaviour. 4. There was no interactive effect of rearing temperature (RT) and trial temperature, but the effect of RT on avoidance behaviour did differ between populations. For an RT of 15 °C, snails from the South Drain (high risk) population showed a more rapid and longer avoidance response than those from the Chilton Moor (low risk) population. In contrast, for snails reared at 20 °C, there was no difference between populations for the duration of the avoidance response and snails from Chilton Moor crawled out faster than those from South Drain. 5. Hence, whilst (predictable) differences relative to natural predation threat in crawl‐out behaviour were apparent at 15 °C, raising the developmental temperature to 20 °C eliminated or, in the case of latency, reversed these differences. This suggests that L. stagnalis populations that cohabit with predatory fish and experience high developmental temperatures may have a reduced ability to respond to fish predation risk.     

Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae)

Some prey can distinguish between chemical cues from predators fed different diets. Here we document the first evidence of diet-based chemical discrimination of predators in a terrestrial arthropod and measure the survival value of behavioural responses to predator chemical cues. We tested activity level and avoidance behaviour of the wolf spider, Pardosa milvina, to faeces and silk associated with the predatory wolf spider, Hogna helluo, fed either P. milvina or crickets (Acheta domesticus). We then measured survival of Pardosa in the presence of Hogna when placed on blank paper or paper previously occupied by Hogna fed either crickets or Pardosa. Filter paper previously occupied by Hogna from each diet treatment or a blank control were simultaneously presented to adult female Pardosa among four treatment pairs (N=15/treatment): (1) blank paper/blank paper, (2) Hogna fed crickets/blank, (3) Hogna fed Pardosa /blank and (4) Hogna fed Pardosa / Hogna fed crickets. Cues from Hogna fed either crickets or Pardosa elicited significantly less activity relative to blank controls. Cues from Hogna fed Pardosa elicited a significantly greater reduction in activity than Hogna fed crickets. When given a choice, Pardosa initially chose the blank substrate significantly more often than either substrate with Hogna cues. Spiders survived longer in the presence of cues from either Hogna diet treatment relative to blank paper, but there was no significant effect of predator diet on survival. Results suggest diet-based predator cues elicit different levels of activity in Pardosa that reduce predation in the presence of Hogna. Copyright 2001 The Association for the Study of Animal Behaviour.     

On the implications of predator avoidance

The question to what extent predators regulate the populations of their food species has a long history of debate, and today top-down control of plankton dynamics still is a major issue in limnology. Over the last decade a fascinating extra dimension of this topic has been revealed. Fish, zooplankton and algae can sense their potential predators through chemical cues and adjust their life style in a flexible way to minimize the risk of being eaten. Although much progress has been made in elucidating the mechanisms involved, the implications of such predation avoidance for the potential of predators to reduce the abundance of their food populations are still poorly understood. Model analyses suggest that predation avoidance leads to more stable food webs in which the effects of nutrient enrichment are more evenly distributed over the trophic levels. In this article it is argued that the cost which predation avoidance usually has in terms of food conditions implies a tricky caveat in interpreting observations on predation rates and nutritional status in natural populations. Prey that sense the presence of predators and aggregates at safe sites where food conditions are poor, may appear starved and actual predation losses may be low. Such observations suggest that food limitation is the dominant force limiting their population development, but although starvation may indeed be the proximate cause of poor growth and reproduction, predation is clearly the ultimate factor involved in this situation. Thus when predation avoidance occurs, standard demographic analyses will tend to underestimate the importance of predators in regulating the dynamics of their prey in the field.     

The ontogeny of antipredator behaviour in paradise fish larvae III. Size-related avoidance of predator models

A series of laboratory experiments examined the effect of the size of predator models on the behaviour of larval paradise fish Macropodus opercularis L., of different age (15 and 20 days old). In a small runway, individually tested larval paradise fish could approach a model predator of different size, with or without eyespots. The duration of approach, the number of fleeings and backings were measured. Fifteen-day-old larvae showed similar moderate level avoidance to all models but fled more in the presence of larger models. The approach behaviour in 20-day-old larvae depended on the size of the model but only if it had eyespots, and larvae fled and backed more with increasing size of the model. However, manipulation of larval length within age category had no effect on predator avoidance. Since the recognition of the two eyespots seems to be age dependent, it is hypothesized that only larvae older than 20 days will behave in a 'threat-sensitive' manner in the presence of predator models by avoiding larger ones.     

Ontogeny of light avoidance in juvenile lake sturgeon

Hatchery‐reared age 1+ and 4+ lake sturgeon (Acipenser fulvescens) were assayed to determine the effectiveness of coloured, strobing LED light guidance device (LGD) at achieving behavioural guidance for attraction or avoidance responses. Based on an initial y‐maze dichotomous choice study in age 1+ fish during daytime, we selected green, blue, orange, and full‐spectrum white light, all strobing at 1 Hz, for further testing. During nighttime light guidance trials, age 1+ sturgeon demonstrated the fastest entries and greatest proportion of entries to the cone of illumination in the experimental raceway when the LGD was producing blue light, and the lowest proportion of entries in response to orange light. Conversely, they also spent the greatest amounts of time under illumination during orange light trials. Blue light was associated with the greatest proportion and total numbers of complete passages through the illuminated zone, although passage rates through this area were observed during the unilluminated control trials. White light resulted in the least time spent in the illuminated zone, and the lowest rates of passage. Under the nighttime testing scenario, the age 4+ sturgeon, by contrast, demonstrated strong avoidance of blue light and white light. While their behaviour was negatively phototactic in general, orange light was the least repulsive. For the behavioural guidance of lake sturgeon moving at night, we recommend the use of blue light strobing at 1 Hz for the attraction of the 1+ age class and white light strobing at 1 Hz for their repulsion. For age 4+ fish, we recommend the use of blue light or white light strobing at 1 Hz for repulsion and caution that (a) light as a behavioural guidance tool appears most effective as a repulsive stimulus, and (b) further testing under both laboratory and field conditions are required.     

Intermediate predator impact on consumers weakens with increasing predator diversity in the presence of a top-predator

Adding or removing a top-predator is known to affect lower trophic levels with potentially large, indirect effects on primary production. However, little is known about how predator diversity may affect lower trophic levels, or how adding or removing a top-predator influences the effects of predator diversity. Using aquatic mesocosms containing three and four trophic levels, we tested whether intermediate predator diversity affected predation on consumers and if top-predator presence influenced such effects. We found that the presence of intermediate predators suppressed the consumer population and that this suppression tended to increase with increased intermediate predator diversity when the top-predator was absent. However, with the top-predator present, increased intermediate predator diversity showed the opposite effect on the consumers compared to without a top-predator, i.e. decreased suppression of consumers with increased diversity. Hence, in our study, the loss of intermediate predator species weakened or strengthened predator–prey interactions depending on if the top-predator was present or not, while loss of the top-predator only strengthened the predator–prey interactions. Therefore, the loss of a predator species may render different, but perhaps predictable effects on the functioning of a system depending on from which trophic level it is lost and on the initial number of species in that trophic level.     

Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish

Animals commonly approach (i.e. 'inspect') potential predators. Glowlight tetras, Hemigrammus erythrozonus, have previously been shown to inspect the combined chemical and visual cues originating from novel predators and to modify their inspection (approach) behaviour depending upon the predator's diet. We conducted two experiments to determine whether tetras would inspect the chemical cues of injured prey or the dietary cues of a novel predator in the absence of any visual cues. Shoals of glowlight tetras were exposed to either distilled water (control) or the skin extract of swordtail (lacking ostariophysan alarm pheromones) or the skin extract of tetra (with alarm pheromones). There was no significant difference in the frequency of predator inspection behaviour towards swordtail or tetra skin extract compared to the distilled water controls. In the second experiment, we exposed shoals of tetras to either distilled water or the odour of Jack Dempsey cichlids, Cichlasoma octofasciatum, which had been food deprived, or fed a diet of swordtails or tetras. There was no significant difference in the frequency of predator inspection behaviour towards the odour of the starved cichlids and the odour of the fed cichlids in either of the two diet treatments. However, when tetras were exposed to the odour of cichlids fed tetras, they took significantly longer to initiate an inspection visit, remained further from the source of the chemical cues and inspected in smaller groups, compared with the odour of a starved cichlid or a cichlid fed swordtails. These data strongly suggest that tetras will inspect chemical cues alone, but only if the cue contains information about the predator. Copyright 2000 The Association for the Study of Animal Behaviour.     

Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits

Predation is a strong selective force with both direct and indirect effects on an animal’s fitness. In order to increase the chances of survival, animals have developed different antipredator strategies. However, these strategies have associated costs, so animals should assess their actual risk of predation and shape their antipredator effort accordingly. Under a stressful situation, such as the presence of predators, animals display a physiological stress response that might be proportional to the risk perceived. We tested this hypothesis in wild European rabbits (Oryctolagus cuniculus), subjected to different predator pressures, in Doñana National Park (Spain). We measured the concentrations of fecal corticosterone metabolites (FCM) in 20 rabbit populations. By means of track censuses we obtained indexes of mammalian predator presence for each rabbit population. Other factors that could modify the physiological stress response, such as breeding status, food availability and rabbit density, were also considered. Model selection based on information theory showed that predator pressure was the main factor triggering the glucocorticoid release and that the physiological stress response was positively correlated with the indexes of the presence of mammalian carnivore predators. Other factors, such as food availability and density of rabbits, were considerably less important. We conclude that rabbits are able to assess their actual risk of predation and show a threat-sensitive physiological response.     

Antipredator behaviour mediated by chemical cues: the role of conspecific alarm signalling and predator labelling in the avoidance response of a marine gastropod

Gastropods represent a challenge in the understanding of alarm signalling. We studied predator avoidance (climbing behaviour) of the marine snail Tegula funebralis in laboratory experiments. Snails were exposed to crude extract of conspecifics, and to water conditioned by actively feeding or non-feeding predatory crabs. Crabs had previously been maintained on different diets, and were accordingly labelled by chemical cues of various origins. Tegula -extract alone released climbing behaviour in May, but not in June. However, during both these months, snails responded to chemical cues from crabs that were actively feeding on Tegula . Crabs labelled by Tegula -diet, and actively feeding on Tegula , also caused more climbing responses compared to crabs labelled by other diets. Chemical cues derived from crabs actively feeding on another snail species, or from non-feeding crabs, did not induce snail climbing no matter the previous feeding history of the predators. When snails received Tegula -extract combined with water conditioned with a non-feeding, Tegula -labelled crab, no climbing occurred. However, when the non-feeding, Tegula -labelled crab was present in the solution of Tegula -extract, moderate climbing responses were obtained. The results imply that climbing responses of T. funebralis are in general caused by the action of a two-component system. This system seems to be a mixture of chemical cues leaking from the tissue of conspecifics when being eaten, and latent conspecific chemicals that are modified in crabs and presumably released with the urine of chemically labelled predators. The modified chemical labels appear to be fully released by crabs when feeding, and moderately released when detecting food. The responses obtained in May with crude extract alone may result from a seasonal change in alarm signalling properties, or a change in behavioural responsiveness of snails exposed to a variable predator regime.     

The effects of group size on predator avoidance in a marine insect

The ocean skater, Halobates robustus (Hemiptera: Gerridae), is a flightless insect which forms loosely aggregated fluotillas of various sizes close to lava and mangrove edges in the Galapagos. Field observations showed a clear effect of group size on the distance at which an approaching predator model induced avoidance behaviour (rapid withdrawal and/or dispersal). It is suggested that in large, highly aggregated groups, the insects are maximally aroused as a result of frequent bodily encounters with adjacent members of the flotilla. An approaching object thus induces avoidance behaviour with minimal visual stimulation at maximal distance. With small groups and single individuals, which are less aroused, a closer approach of the object is required to produce visual stimulation sufficient to activate the escape response.