Do inter- and intraspecific aggression vary in relation to predation pressure in sticklebacks?

The relative abundance of predatory fish at 15 sites was assessed and the reactions of stickle-backs (Gasterosteus aculeatus) collected from these sites to a hunting pike (Esox lucius) and a breeding conspecific were measured. Both the degree of boldness shown towards a pike and the level of aggression shown towards conspecifics varied significantly between sites; sticklebacks coexisting with abundant predators showed the lowest level of both these responses, but this was less clear-cut in the case of intraspecific aggression.     

Effects of perceived predation risk and social environment on the development of three‐spined stickleback (Gasterosteus aculeatus) morphology

Phenotypically plastic changes in response to variation in perceived predation risk are widespread, but little is known about if and how social environment modulates induced responses to predation risk. We investigated the influence of perceived predation risk (i.e. chemical cues from a predator) and social environment (i.e. one, two or 20 individuals reared together) on three‐spined stickleback (Gasterosteus aculeatus) morphology in a factorial common garden experiment. We found that exposure to chemical cues from potential predators did not influence growth or body condition or induce more robust morphological defences (i.e. lateral plate numbers and dorsal spine lengths). However, sticklebacks exposed to predator cues developed longer caudal peduncles and larger eyes as compared with fish from the control treatment. As these responses may improve sticklebacks’ ability to avoid piscine predation, they might be adaptive. Social environment/density also influenced expression of some traits, but these effects were independent of predation‐risk treatment effects. In general, these results suggest that apart from the classic morphological defence structures, which appear mostly constitutive, three‐spined sticklebacks are capable of expressing potentially adaptive morphological responses to chemical cues from potential predators.     

Agonistic Interactions in Juvenile Sticklebacks (Gasterosteus aculeatus) in Relation to Local Predation Risk

Size-matched groups of three-spined stickleback (Gasterosteus aculeatus) fry were established using fish from two sites, one with abundant piscivorous predators (the high-risk site) and the other with very few heterospecific predators (the low-risk site). Over a period of two months, social interactions within groups were monitored regularly and mean lengths and coefficients of variance in length were tracked. Agonistic behaviour was observed in 45% of observation periods, but was more common in the groups of fry from the low-risk site, where it was more likely to take the form of direct attack rather than displacement without contact. In both categories of fish, the great majority of agonistic acts were directed to fish of a similar size or smaller. Mean size increased rapidly in all groups. At the same time, the coefficient of variation also increased, approaching 15% after two months in both categories of fish, reflecting differing growth rates among individuals. After three months, the two largest and the two smallest fish from each group were observed individually during an encounter with a model predatory fish. Large and small fish from both sites behaved identically in this test, suggesting that in sticklebacks (unlike guppies, for example) early experience of aggressive attacks from conspecific companions may not influence the development of anti-predator responses. As has been reported previously, sticklebacks from the high-risk site responded much more strongly than low-risk fish.     

Brood Value and Life Expectancy as Determinants of Parental Investment in Male Three-spined Sticklebacks,Gasterosteus aculeatus

29 breeding male three-spined sticklebacks (Gasterosteus aculeatus) caught in the wild at different times in the breeding season were exposed simultaneously to a potential threat to their nest (a conspecific male) and to two hunting trout (potential predators of adult sticklebacks, seen through a transparent partition). By promoting a variety of protective responses, the presence of the predators reduced both the time spent confronting the intruder and the rate at which it was attacked. Subjects with a clutch of eggs in their nest maintained higher levels of territorial defence in the presence of predators than did those with an empty nest. However, those breeding later in the season took fewer risks to defend their nest. Possible proximate mechanisms responsible for these results are discussed. In addition, the adaptive significance of the behavioural changes is considered in the light of the value of the brood and the expected future reproductive output of the sticklebacks breeding at different times in the season.     

A comparison of the behavioural responses of parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia

Eighty sticklebacks (32 parasitized, 48 uninfected) were subjected to a serial reduction in dissolved oxygen (DO) concentration until they showed continuous aquatic surface respiration for longer than 10s (> 10s ASR). An analysis of results showed that (1) parasitized adult male and female sticklebacks reacted to low DO significantly earlier than non-parasitized controls; (2) severity of parasite infection was significantly correlated with DO at which > 10s ASR occurred; (3) gravid, non-parasitized females show ASR at a relatively high DO, with a threshold response similar to that of parasitized fish.
It is suggested that the metabolic respiratory demand of the parasitic tapeworm larvae causes the stickleback to modify its behaviour at lowered DO. This behavioural modification causes the fish to surface, where they are likely to be at risk from predatory birds. Field data on DO levels at the study site show that environmental conditions in the shallow lake margins approach the range required to affect the behaviour of heavily parasitized sticklebacks.     

Age,Experience and the Development of Adaptive Variation in Anti-predator Responses in Three-spined Sticklebacks (Gasterosteus aculeatus)

Stickleback fry (approx. 10 mm in length) were collected from two sites in Scotland, one with abundant predatory fish and birds and the other free of predation. The fry were reared in the laboratory until they reached a length of about 30 mm, at which time fry of the same length were caught from the two study sites. 10 fish from each size and rearing category (10 mm fry, 30 mm labreared fry and 30 mm wild-caught fry) and from each population were exposed singly to a silhouette of an avian predator moved above the surface of the tank. On average 50% of the fish jumped away on sighting the model, and there were no differences between the groups in the proportion of fish giving this response. Other aspects of the anti-predator repertoire of sticklebacks (in particular, remaining motionless after an encounter) were absent in 10 mm fry from both sites. Protective responses appeared (in fish from the predated but not the unpredated site) by the time they reached a length of 30 mm, regardless of whether they were laboratory-reared or wild-caught. Thus adaptive behavioural differences between these two populations arise as sticklebacks from the heavily predated site develop responses that fail to appear in those from the unpredated site and that are independent of direct experience of predatory attack.     

Comparison of taste preferences in the three-spined Gasterosteus aculeatus and nine-spined Pungitius pungitius sticklebacks from the White Sea Basin

Similarity between the taste preferences of classical taste substances and free L-amino acids in adult three-spined stickleback Gasterosteus aculeatus (forma leiurus) and nine-spined stickleback Pungitius pungitius (forma laevis) was found. The strongest and the most significant responses in both species were evoked by citric acid and cysteine, asparatic, and glutamic acids. Sodium chloride, calcium chloride, sucrose, and the remaining 18 amino acids do not elicit a statistically significant effect on the consumption of agar-agar pellets by the fish or have weak taste attractiveness. Similarity of taste preferences in the three-spined and nine-spined sticklebacks are supported by correlation analysis. Absolute values of the consumption of pellets of the same types are also similar in the two species. There were, however, differences in the behavioral taste response, repeated snaps, and the duration of processing of the pellets. The taste response of the nine-spined stickleback is more similar to taste responses in fish of the limnophilic complex than to the response in the three-spined stickleback. It is hypothesized that taste spectra may be very similar in fish with similar ecology and feeding patterns not only in sticklebacks, but also in other related species.     

Development of the overhead fright response in wild and predator-naive three-spined sticklebacks, Gasterosteus aculeatus L.

Variation in the overhead fright response within populations between adult and juvenile sticklebacks and between juveniles from separate populations are described. The development of the response was measured experimentally in fish from two populations subject to avian predation and in predator-inexperienced fry from one of these populations. The response developed with age and/or body size. The even development of the response in a sample of laboratory-reared fry suggests that experience of predators is not necessary for the normal development of this behaviour.     

Feeding and Avoiding Predation Hazard: the Behavioral Response of the Prey

A forager may respond to the hazard of predation by (1) ignoring the hazard and eating maximally at all levels of food (risk-reckless); (2) avoiding the hazard and minimizing eating (risk-avoiding); (3) reducing feeding by the same amount at each level of food, making greater reductions as hazard increases (risk-adjusting); (4) reducing feeding at low levels of food, while accepting a greater hazard when food levels are high (risk-balancing). We experimentally distinguished these four nominal responses using 9 three-spined sticklebacks, Gasterosteus aculeatus in a 3 times 4 factorial, repeated measures design. The fish were tested in an aquarium containing a refuge inaccessible to predatory trout, Salmo trutta, in 12 combinations of food (low, medium, high) and predation hazard (predator density = 0, 1, 2, 3). With predators, sticklebacks ate less and used the refuge more. Amount eaten, but not time spent out of the refuge, was positively correlated with food, even in the absence of predators. Since sticklebacks as a group appeared to depress feeding by equal amounts at all levels of food, they employed a risk-adjusting response. However, individuals varied in their response to hazard.     

Fishing spiders, green sunfish, and a stream-dwelling water strider: male-female conflict and prey responses to single versus multiple predator environments

Many studies have experimentally addressed the effects of a particular predator species on prey behavior. In nature, however, prey frequently face multiple species of predators that often vary in their predatory mode and in their level of predation risk. Relatively few studies have considered prey responses under these complex conditions. In Kentucky, the stream-dwelling water strider (Aquariusremigis) coexists with many potentially dangerous predators, two of which are the green sunfish (Lepomiscyanellus) and the fishing spider (Dolomedesvittatus). Green sunfish occupy stream pools and attack water striders from below. In contrast, fishing spiders hunt along stream shorelines where they perch on overhanging vegetation or rocks and attack water striders near shore. We compared how A. remigis individuals respond to these two very different predators in pools with one or both predators. The presence of sunfish in pools had strong effects on male water strider behavior, including increased use of three types of refuge from sunfish (riffles, climbing out of the water, sitting on the water but at the edges of pools), decreased activity and a decreased number of aggressive males on the water. Spiders also influenced water strider behavior; male water striders avoided spiders by shifting away from the edges of pools. Comparisons of the effects of the two predator species showed that in general, antipredator responses by male water striders were stronger in pools with fish alone than in those with spiders alone. In the presence of both predators, male water strider behavior (microhabitat use and activity) was generally similar to behavior in the presence of fish alone. In contrast, female water striders showed no significant response to the presence of sunfish, and little response to the presence of spiders. This lack of response could be because females spent much of their time in refuges even in the absence of predators (apparently hiding from harassment by males). Both spiders and fish caused decreases in water strider mating activity. The presence of fish reduced both the number of matings per pool (mating frequency), and mean mating durations. Spiders induced a decrease in mean mating duration, but not in mating frequency. The largest reductions in mating activity occurred in pools with both predators present. Pools with either spiders or fish alone suffered 15–20% water strider mortality during our experiment (versus no mortality in predator-free pools). Extant theory suggests that when prey face conflicting microhabitat responses to two predators (as in this study), the predators should have facilitative effects on predation rates (i.e., prey that avoid one predator are often killed by the other and vice versa). Mortality rates in pools with both predators present, however, were not significantly different from that predicted by a null model of multiple predator effects. The lack of predator facilitation can be explained by the compensatory reductions in water strider activity and mating activity in the presence of both predators. Received: 26 August 1996 / Accepted: 12 June 1998     

Antipredator Behavior of American Bullfrogs (Lithobates catesbeianus) in a Novel Environment

Invasive species capable of recognizing potential predators may have increased establishment rates in novel environments. Individuals may retain historical predator recognition and invoke innate responses in the presence of taxonomically or ecologically similar predators, generalize antipredator responses, or learn to avoid risky species in novel environments. Invasive amphibians in aquatic environments often use chemical cues to assess predation risk and learn to avoid novel predators via direct experience and/or associated chemical cues. Ontogeny may also influence recognition; experience with predators may need to occur at certain developmental stages for individuals to respond correctly. We tested predator recognition in invasive American bullfrog ( Lithobates catesbeianus) tadpoles that varied in experience with fish predators at the population and individual scale. We found that bullfrog tadpoles responded to a historical predator, largemouth bass ( Micropterus salmoides), only if the population was locally sympatric with largemouth bass. Individuals from a population that did not co‐occur with largemouth bass did not increase refuge use in response to either largemouth bass chemical cues alone or chemical cues with diet cues (largemouth bass fed bullfrog tadpoles). To test whether this behavioral response was generalized across fish predators, we exposed tadpoles to rainbow trout ( Oncorhynchus mykiss) and found that tadpoles could not recognize this novel predator regardless of co‐occurrence with other fish species. These results suggest that environment may be more important for predator recognition than evolutionary history for this invasive species, and individuals do not retain predator recognition or generalize across fish predators.     

Are behavioral responses to eyespots in sticklebacks influenced by the visual environment? An experimental examination

Eyespots are taxonomically widespread color patterns consisting of large concentric rings that are commonly assumed to protect prey by influencing the behaviors of predators. Although there is ample experimental evidence supporting an anti‐predator function of eyespots in terrestrial animals, whether eyespots have a similar deterring function in aquatic animals remains unclear. Furthermore, studies in terrestrial systems suggest that the protective function of eyespots depends on ambient light conditions where predators encounter them, but this effect has never been tested in aquatic environments. Here, we examine how eyespots influence behavioral responses in an aquatic environment under different visual environments, using laboratory‐reared three‐spined sticklebacks (Gasterosteus aculeatus) as model predators. Specifically, we experimentally examined behavioral responses of sticklebacks toward artificial prey patterns (control vs. eyespots) under two different light environment treatments (low vs. high). We found that eyespots did not postpone attacks from sticklebacks. However, sticklebacks approaching eyespots stopped more frequently than sticklebacks approaching prey items with a control pattern. Sticklebacks were (marginally) slower to attack prey in the low‐light treatment, but the light level did not influence stickleback behavioral responses toward eyespots. We conclude that eyespots can modulate some behaviors of an aquatic predator, albeit with a different functional role from that previously demonstrated in terrestrial species.     

Female bias in the adult sex ratio of African annual fishes: interspecific differences,seasonal trends and environmental predictors

Many populations have consistently biased adult sex ratios with important demographic and evolutionary consequences. However, geographical variation, the mechanisms, temporal dynamics and predictors of biased sex ratios are notoriously difficult to explain. We studied 334 wild populations of four species of African annual fish (Nothobranchius furzeri, N. kadleci, N. orthonotus, N. rachovii) across their ranges to compare their adult sex ratio, its seasonal dynamics, interpopulation variation and environmental predictors. Nothobranchius populations comprise a single age cohort and inhabit discrete isolated pools, with wide-ranging environmental conditions (habitat size, water turbidity, structural complexity, predators), making them ideal to study adult sex ratio variation. In captivity adult sex ratios were equal. In natural populations, adult sex ratios were biased 1:2 toward females in three study species while N. kadleci had sex ratios at unity. There was a decline in the proportion of males with age in one species, but not in the other species, implying most severe male mortality early after maturation, declining later perhaps with a decrease in male abundance. In general, the populations at vegetated sites had relatively more males than populations at sites with turbid water and little vegetation. Selective avian predation on brightly coloured male fish likely contributed to female dominance and vegetation cover may have protected males from birds. In addition, an aquatic predator, a large belastomid hemipteran, decreased the proportion of males in populations, possibly due to greater male activity rather than conspicuous colouration. Alternative explanations for a sex ratio bias, stemming from male–male contests for matings, are discussed. We conclude that the effect of environmental conditions on adult sex ratio varies dramatically even in closely related and ecologically similar sympatric species. Therefore, difficulties in explaining the ecological predictors of sex ratio biases are likely due to high stochasticity rather than limited sample size.     

Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: Population and sex differences

Aggression is often positively correlated with other behavioural traits such as boldness and activity levels. Comparisons across populations can help to determine factors that promote the evolution of such traits. We quantified these behaviours by testing the responses of wild-caught poeciliid fish, Brachyrhaphis episcopi, to mirror image stimuli. This species occurs in populations that experience either high or low levels of predation pressure. Previous studies have shown that B. episcopi from low predation environments are less bold than those that occur with many predators. We therefore predicted that fish from high predation populations would be more aggressive and more active than fish from low predation populations. However, we found the opposite - low predation fish approached a mirror and a novel object more frequently than high predation fish suggesting that ‘boldness’ and aggression were higher in low predation populations, and that population-level boldness measures may vary depending on context. When tested individually, low predation fish inspected their mirror image more frequently. Females, but not males, from low predation sites were also more aggressive towards their mirror image. Variation in female aggression may be driven by a trade-off between food availability and predation risk. This suggests that the relationship between aggression and boldness has been shaped by adaptation to environmental conditions, and not genetic constraints.     

Antipredator response of pea aphids <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis> (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch

To escape from predators, herbivorous prey could leave their current patch and relocate to an alternative patch. However, when other predators are present on the new patch, prey are again exposed to predation risk. Thus, patch leaving might be affected by the other predators. We studied patch leaving of pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in response to ladybird larvae Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on broad bean Vicia faba L. shoots that were offered as patches for aphids. We tested whether shoot leaving was affected by the presence of predators on alternative shoots under laboratory conditions. Odors from alternative shoots were evaluated as possible cues used by aphids to assess predation risk on the shoots. We exposed aphids to odors from alternative shoots with conspecifics plus either adult or larval ladybirds or larval green lacewings Mallada desjardinsi Navas (Neuroptera: Chrysopidae). Shoot leaving was reduced only when adult ladybirds were present on the alternative shoots compared with controls (i.e., no predators on the alternative shoots). Odors of both adult ladybirds and of conspecifics being attacked by ladybird larvae were required for reduced leaving. Hence, predation risks on current and alternative patches might affect the antipredator responses of aphids.     

Predation risk and the opportunity for female mate choice in a coral reef fish

The influence of predation risk on the opportunity for female mate choice was investigated in the tailspot wrasse Halichoeres melanurus at two sites on a coral reef in Okinawa, Japan. Females mated repeatedly with the nearest males, but they also changed mates frequently at both sites. Mate changes were seen not only in the context of spatiosocial changes (mate disappearance or shifts in male territories) but were also probably the result of actual mate choice by females. Females at one site (site A) changed mates more often and conducted longer spawning trips from their home ranges to male territories than at the other site (site B). Fish at site A were faced with a higher frequency of predators than that of site B. However, fish of site A suffered fewer attacks from predators because they had more shelter, suggesting lower predation risk in that site. These results suggest that females under higher predation risk had less opportunity to choose preferable mates and that they had to mate with the same, nearest males in most cases.     

Algal Turbidity Reduces Risk Assessment Ability of the Three‐Spined Stickleback

Recent anthropogenic increases in algal turbidity in aquatic habitats have been suggested to affect the ability of fish to assess predation risk. We investigated the response of feeding three‐spined sticklebacks (Gasterosteus aculeatus) exposed to a sudden appearance of an avian predator (the silhouette of common tern, Sterna hirundo), under clear and turbid water conditions. As stickleback use social cues to aid in predator avoidance, we also tested whether turbidity affected social information use by manipulating group size. We found that in turbid water, a smaller proportion of fish would escape from the feeding area, that the distance escaped was shorter and that a smaller proportion of fish fled into shelter. Larger group size was associated with longer escape distance and greater shelter use. However, there was no effect of group size on the proportion of fish that escaped the arena. The effect of group size was similar for turbid and clear water. Our finding that the fish showed a weaker antipredator response suggests that turbidity impedes their risk assessment capability. However, the sticklebacks were still able to benefit of the social facilitation provided by being in a group. This suggests that algal turbidity has detrimental effects on the ability of sticklebacks to assess predation risk from avian predators in shallow water. An implication is that in shallow water fish may be more vulnerable to avian predation under turbid conditions.     

Within-group variation in the willingness to risk exposure to a predator: the influence of species and size

The costs and benefits associated with feeding in the vicinity of a predator should vary within and among species, depending on an individual's vulnerability to a predator. In this paper, we investigate how willingness to risk exposure to a predator in order to gain access to food is expressed within groups of fish. We provided groups of six individually marked brook sticklebacks ( Culea inconstans ) and fathead minnows ( Pimephales promelas ) with the opportunity to feed in safety, or in the presence of a single predator (walleye, Stizostedion vitreum ). Sticklebacks and fathead minnows are commonly found in the same locations at the same time, but sticklebacks also possess armour and spines that provide defence against some predators. Despite this morphological variation, patterns of individual behaviour were consistent between species. While feeding close to the predator, there was a positive relation between the size of the individual and the proportion of food consumed. No relation existed on the side farthest from the predator. These data suggest that fish may risk exposure to predators to exploit size-related differences in vulnerability to gain a competitive advantage for access to food.     

The influence of gummy sharks, Mustelus antarcticus, on observed fish assemblage structure

Large predatory fish that alter the behaviour of smaller species may affect visual estimates of abundance by making organisms more or less difficult to observe and quantify. To evaluate the non-consumptive influence of large predators on rocky reef fishes observed with Baited Remote Underwater Video (BRUV), we tested the hypothesis that fish assemblages monitored when large (ca 1.5 m) piscivorous sharks, Mustelus antarcticus, were present differ from those observed when sharks were absent. We did this in two ways using recordings from rocky reefs in Batemans Marine Park, NSW, Australia. First, we examined 6 min of each 30 min tape; 3 min when sharks were present and 3 min when they were absent, in a paired sample design from 17 sites. Second, we compared fish assemblages for complete tapes (30 min) at sites with sharks present compared to sites where they were absent. The diversity and total abundance of fishes was consistently lower in the presence of sharks; we detected significant assemblage-wide change (PERMANOVA, P?<?0.05). Importantly, the diversity and total abundance of fishes for complete tapes (30 min) decreased in the presence of sharks by 18 % and 36 %, respectively, underscoring the likelihood that sharks influence observed fish assemblages. Individual species responses were variable and while the abundance of many fish species decreased in response to sharks, others increased 6-fold. Overall, these results highlight the need to consider systematic differences in the abundance of large predators to avoid biases when testing hypotheses about fish assemblages using non-destructive visual methodologies.     

Altered Prey Responses in Round Goby from Contaminated Sites

Although prey must move to forage, escape predation or gain information about predation risk, movement itself enhances the risk of predation by increasing visibility of prey and encounter rates with predators. Animals subjected to stressors often show altered behaviour; a widely cited effect of contaminant exposure is an increase in vulnerability to predation, which may be mediated by an increase in risky behaviour. Round goby are invasive fish that typically rely on crypsis and sheltering (low‐activity behaviours) to avoid predators. We collected round goby from contaminated sites and tested whether they showed signs of altered risk‐taking compared with fish from a less contaminated reference site. We subjected the fish to a simulated predation event (a motor‐operated model bass) under both diurnal and nocturnal conditions. Fish from contaminated sites showed lower overall activity levels, but also failed to reduce activity following an attack, unlike fish from the reference site. The intensity of effects varied with diel period. Males, but not females, from contaminated sites showed reduced likelihood of darting during an attack, while females, but not males, from contaminated sites were less likely to approach the predator. Sex differences in round goby risk‐taking may reflect sex‐specific selection pressures on activities promoting predation risk. With the exception of post‐attack activity, round goby from contaminated sites generally showed signs of reduced risk‐taking. If contaminant exposure increases goby vulnerability to predators, it may be occurring through behavioural mechanisms other than impacts on risky prey responses.