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.     

Predation risk and inter-population variation in antipredator behaviour in the three-spined stickleback, Gasterosteus aculeatus L.

Predation risk from fish and bird predators was assessed at seven Scottish Gasterosteus aculeatus L. sites. Samples of adult male and female sticklebacks and fry from each site were tested with either a model heron or a live pike to measure anti-predator responses. Principal Component Analyses were then used to describe the responses, the first factor to emerge from each multivariate analysis providing an index of overall level of response toward the predator. Significant sexual and inter-population differences in behaviour are described. Sticklebacks from populations at high risk from either predatory fish or birds showed higher fright response scores than fish from low risk sites. In general, adult male sticklebacks are bolder than adult females during interactions with predators.     

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.     

Anthropogenic risk increases night-time activities and associations in African elephants (Loxodonta africana) in the Ruaha-Rungwa ecosystem,Tanzania

Elephants face diverse threats from human activities and use temporal and social strategies to reduce human-induced mortality risk. We used data from camera trap surveys in 2018–2019 (n = 1625 independent detection events from 11,751 sampling days) to investigate elephant responses to anthropogenic risk in the Ruaha-Rungwa ecosystem, Tanzania. The study was conducted in one low-risk and three high-risk sites using 26–40 paired camera trap stations per site. Risk influenced the active periods, use of roads and water sources, social associations and behaviour of elephants. Elephants demonstrated significantly more night-time and reduced daytime activity in the high-risk sites relative to the low-risk site. This higher night-time activity in the high-risk sites was observed for both males and females, though it was more pronounced for cow–calf groups than lone males. Foraging events and use of water sources were more frequent at night in the high-risk sites. Elephants used roads as movement routes in the low-risk site but avoided roads in the high-risk sites. Males were significantly more likely to associate with other males and cow–calf groups in the high-risk sites. Fewer occurrences of relaxed behaviours were observed in the high-risk sites compared to the low-risk site. We discuss the potential implications of our findings for elephant survival and reproduction.     

Measuring the cost of reproduction

Gravid and barren Daphnia pulex were exposed to a variety of predators in laboratory aquaria. Small fish (guppies, sticklebacks and shiner fry) consistently preferred the gravid females, establishing the existence of a behavioural cost of reproduction. However, no such cost was associated with predation by more efficient visual predators (sunfish) or by nonvisual predators (hydras), and the excess of gravid females eaten by backswimmers was found to be attributable to their distribution in the water column. Moreover, the cost associated with predation by small fish was observed only when the Daphnia were presented against a light background, and was abolished when a dark background was substituted. In a further series of experiments with guppies we attempted to show that each egg added to the brood caused a decrease in survival; in two such experiments survival rate was related to body size but not to fecundity, while in a third the effect of body size did not appear, and a negative correlation between survival and fecundity could be demonstrated. Although these experiments unambiguously demonstrate a cost of reproduction they also illustrate the elusiveness of the phenomenom and emphasize the need to develop theories which specify the type and magnitude of costs generated by different ways of life.     

Group Choice as a Function of Group Size Differences and Assessment Time in Fish: The Influence of Species Vulnerability to Predation

The shoal-choice behaviour of two species of fish that differ in their vulnerability to predation was compared. Individuals of threespine stickleback, Gasterosteus aculeatus, and creek chub, Semotilus atromaculatus, were presented with a simultaneous choice of two equidistant stimulus shoals of conspecifics that differed in membership size (5 vs. 6 fish, 5 vs. 7, 5 vs. 8, 5 vs. 9 and 5 vs. 10). Test fish were allowed to view the stimulus shoals from a standard distance for either 10–20 or 120–150s before being frightened with a stimulus from an overhead light and released to join either shoal. We observed which shoal (the smaller or the larger one) the test fish approached. Preference for the larger stimulus shoal generally increased with increasing shoal size difference and with the duration of the assessment period, and was more pronounced in chub (the more vulnerable of the two species). For the short assessment period, chub showed a significantly stronger preference for the larger stimulus shoal than sticklebacks, whereas there was no significant difference between species for the long assessment period. Furthermore, chub responded more readily to small differences in shoal size (of 1–3 fish) than sticklebacks, for both short and long assessment periods. The above results are consistent with the hypothesis that chub, as the more vulnerable of the two species (in terms of predation), should be able to identify the larger of two shoals more quickly and should be more sensitive to small differences in shoal size than sticklebacks.     

Schooling affects growth in the three-spined stickleback, Gasterosteus aculeatus

Three-spined stickleback fry (mean length 20 mm, mean weight 14 mg) were reared for 14 days alone and in groups of six in a constant per capita water volume. The fish originated from two habitats (rock-pools, sea) of different predation pressure. The fry were fed nauplii of Artemia and commercial aquarium fish food ad libitum. Specific growth rates of solitary and schooling fry differed and were also affected by their origin. The specific growth rates of solitary fry from the sea averaged 1.0% day⁻¹ (length) and 6.0% day⁻¹ (weight) and those of solitary rock-pool fry 1.1 and 6.7%, respectively. For group-reared fish the corresponding values were 1.2% (length) and 6.6% (weight), and 1.3% (length) and 7.6% (weight). The finding that schooling sticklebacks grow faster than solitary ones implies that grouping enhances fitness in stickleback fry under the conditions of our experiments.     

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.     

Shadow competition in wild juvenile sea-trout

Shadow competition occurs in a group of sit-and-wait predators when those closer to a source of mobile prey reduce the feeding success of those further from the prey source. It was examined in territorial juvenile sea trout Salmo trutta in a small stream. The fry formed groups of two to six fish with adjacent territories and a social hierarchy within each group. It was hypothesized that: (i) as group size increased, the mean number of prey eaten per fish within a group decreased and the variability in prey consumption between fish increased; (ii) prey consumption by individual fish decreased with increasing distance from the food source; (iii) group size increased as the mean water velocity immediately upstream from a group, and hence potential drifting food, increased. Five groups of fry were fed on small shrimps released upstream from each group at a rate of one every 15 s over a 10 min period, this procedure being repeated over 5 days to provide five replicates per group. Experiments were performed three times in 1967, 1969 and 1974 to provide information on 45 groups of fry. The first and third hypotheses were supported, but the second was only partially supported. In 1967 and 1969, territory size and shrimp consumption by individual fry decreased with increasing distance from the food source. This also occurred in 1974, except during a critical period for survival when fry density was exceptionally high with large numbers of sea trout lacking territories. This resulted in sea trout fry with the largest territories eating fewer shrimps than those with medium-sized territories because they spent more time defending their territories against sea trout lacking territories. This study is the first to demonstrate shadow competition in a vertebrate species, but has also shown that territorial defence may modify the consequences of shadow competition when densities are high and there is strong competition for the acquisition of a territory.     

First access to territorial space and exposure to strong predation pressure: A conflict in early emerging Atlantic salmon (Salmo salar L.) fry

Summary This work aimed to elucidate conflicting factors that may explain the narrow and synchronous emergence in salmonids. Fry are highly vulnerable to predation and stand a better chance of surviving if they emerge synchronously. On the other hand, fry that leave the gravel first should increase their chance of obtaining one of the limited number of feeding territories. The risk involved in early emergence for Atlantic salmon fry was evaluated by exposing them to predatorySalmo trutta. Yolk sac alevins were incubated in an artificial redd in order to catch them by their time of emergence. Early-, peak- and late-emerging fry were then successively marked and transferred to flume tanks in which the predators were either present from the start or not introduced until all fry had been added. When the predators were initially present, the predation pressure differed depending on the time of fry emergence, resulting in survival rates of 11.6, 44.9 and 51% in early-, peak- and late-emerging fry, respectively. By assuming that the predation rate of the three emergence groups was dependent both on time of emergence and fry density the survival rates were calculated to be 7.5, 41.1 and 53.5% in groups I, II and III, respectively. These figures corresponded well to the observed rates. When the predators were added after completed emergence the resulting survival rates were 56.9, 39.7 and 25.2% in early-, peak- and late-emerging fry, respectively. Thus, predation after complete emergence gave a survival probability that varied across the three emergence-date groups, despite being exposed to a predator during the same number of days. The presence of fish predators in combination with a limited territorial space seems to make both early and late emergence hazardous and favours synchronous swimming movements.     

Overriding the oddity effect in mixed-species aggregations: group choice by armored and nonarmored prey

Because "odd" individuals often suffer disproportionately highrates of predation, solitary individuals should join groupswhose members are most similar to themselves in appearance.We examined group-choice decisions by individuals in armoredand nonarmored species and predicted that either (1) the oddityeffect would result in preference for conspecific groups forsolitary individuals of both species, or (2) individuals inthe armored species would prefer to associate with groups containingindividuals of the more vulnerable species. Armored brook sticklebacks(Culaea inconstans) and nonarmored fathead minnows (Pimephalespromelas) have the same predators and often occur together instreams. In mixed-species shoals, yellow perch (Perca flavescens)attacked minnows earlier and more often than sticklebacks. Wetested whether solitary minnows and sticklebacks preferred toassociate with conspecific or heterospecific shoals under conditionsof both low and high predation risk. When predation risk washigh, minnows preferred to associate with conspecifics overheterospecifics, as predicted by the oddity effect. In contrast,sticklebacks preferentially associated with groups of minnowsover groups of conspecifics when predation risk was high. Whenpredation risk was low, solitary individuals of both speciespreferentially associated with conspecific over heterospecificshoals. Stickleback shoal choices under low-risk conditionsmay have been influenced by interspecific competition for food.In feeding experiments, minnows were more efficient foragersthan sticklebacks, so it should benefit sticklebacks to avoidminnows unless predation risk is high. Therefore, for armoredprey, the benefits of associating with more vulnerable preyappear to override the costs of both the oddity effect and foodcompetition when predation risk is high.     

Reproductive and histopathological effects of long-term experimental exposure to bis(tributyltin)oxide (TBTO) on the three-spined stickleback, Gasterosteus aculeatus Linnaeus

Three-spined sticklebacks, Gasterosteus aculeatus Linnaeus, were exposed to 0, 0.1, 1.0, 2.5 and 10 μg bis(tributyltin)oxide (TBTO) 1⁻¹ for up to 7.5 months in a flow-through system of sea water. As early as 4 weeks after the start of the experiment, fish from the 10 μg TBTO 1⁻¹ group showed diminishing appetite, increasing lethargy and opaque eyes. The mortality in this group after 2 months of exposure was 80%. No significant differences between the control and the exposed groups were noted concerning fecundity, hatched fry and frequencies of malformed fry. The gonad somatic index (GSI) was determined before and during the spawning period. GSI in control fish increased significantly, while that in the exposed groups remained unchanged between the two sampling occasions. Structural examination of the gills from fish exposed for 2 months to 10 μg TBTO I⁻¹ revealed fusion between secondary lamellae and gradual cell degeneration. The chloride cells were characterized by degenerating mitochondria. Hepatocytes in fish exposed to 2.5 and 10 μg TBTO I⁻¹ contained an increased number of lipid-containing vacuoles and the nucleoli were disorganized and fragmented.     

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.     

Diel vertical movements,and effects of infection by the cestode <Emphasis Type="Italic">Schistocephalus solidus</Emphasis> on daytime proximity of three-spined sticklebacks <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis> to the surface of a large Alaskan lake

We conducted a field study in Iliamna Lake, Alaska, to test the hypothesis that proximity of three-spined sticklebacks Gasterosteus aculeatus to the lake’s surface during the daytime varies with macroparasitic cestode parasite Schistocephalus solidus infection in a manner consistent with enhanced vulnerability to avian predators. Extensive sampling in the lake and likelihood-based modeling revealed that sticklebacks displayed a diel vertical migration, being closer to the surface at night than during the evening and early morning. Additional sampling, also coupled with a likelihood-based modeling approach, showed that fish caught at the surface of the lake during the day were more often parasitized (76 vs. 65%), more heavily parasitized (26.8 vs. 22.7% of their body mass), and had larger individual parasites (0.24 vs. 0.20 g) than those caught at night. Parasite infection was related, non-linearly, to fish size, which also differed between day and night sampling at the surface. We performed statistical competitions among nested hierarchies of models that accounted for this effect of length. The most likely models indicated that fish captured during the day had greater parasite prevalence, higher parasite burdens, and larger parasites than did fish captured at night. Proximity to the surface during the day in this very clear lake would likely increase the vulnerability of sticklebacks to predation from birds, enabling completion of the parasite’s lifecycle.     

Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild

The feeding ecology of three piscivorous fish species (perch (Perca fluviatilis), pike (Esox lucius) and burbot (Lota lota)), was studied in the subarctic Pasvik watercourse (69 °N), northern Norway and Russia. All three species primarily occupied the benthic habitats in the watercourse. Perch and burbot exhibited distinct ontogenetic niche shifts in food resource use, perch changing from a dominance of zooplankton to zoobenthos to fish, and burbot from zoobenthos to fish. Fish prey dominated the diet of all the investigated size-classes of pike, but small-sized pike (<20 cm) were not represented in the sample. Fish prey size was positively related to predator size in all three species. Whitefish (Coregonus lavaretus) was the dominant prey of pike and large-sized burbot and perch. Nine-spined sticklebacks (Pungitius pungitius) was also an important prey and appeared to be a dietary stepping-stone enhancing the transition from invertebrate feeding to consumption of large-sized whitefish prey for all three predators. A cluster analysis separated the different size groups of the three predator species into five functional feeding groups, most of them containing two or all three species. Within these feeding groups, and especially among the piscivorous size-classes, there was a strong and significant interspecific overlap in prey selection, and the dietary similarities between the species were in general much larger than the intraspecific similarities between ontogenetic stages. All three piscivorous species are important top predators in the aquatic food web of the watercourse, and their ontogenetic diet shifts and resource partitioning patterns generate a substantial food web complexity in this subarctic ecosystem.     

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.     

Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection

This paper describes the results of a study of the effects of Schistocephalus solidus on one of its intermediate hosts, the stickleback Gasterosteus aculeatus , in an annual population in which infection is known to occur in one major wave in autumn. Weight, as a function of length, was lower in infected sticklebacks compared with uninfected fish during autumn and spring; in winter and summer, both categories of fish were in equally poor condition. In early autumn, the hepatosomatic indices of newly infected fish were higher than those of uninfected fish, perhaps due to a pathological response. Thereafter, relative liver size of uninfected and infected sticklebacks was comparable until spring, when it increased sharply in uninfected sticklebacks but remained stable at a low level in infected sticklebacks. Few infected fish reached maturity. The only males to attain maturity whilst sustaining an infection of S. solidus were in particularly good condition. Nuptial coloration, kidney hypertrophy and testes size were unimpaired in these mature infected males, but whether they were capable of successful reproduction remains debatable.     

The impact of three-spined sticklebacks on the Zooplankton of a previously fish-free pool

SUMMARY.

• 1 In the Camargue (southern France), most invertebrates inhabiting temporary shallow oligohaline marshes and pools are large-bodied, conspicuous and defenceless taxa that are restricted to fish-free environments. Management practices, by creating drainage canals, strongly affect the invertebrate community by allowing colonization by fish.
• 2 Sticklebacks colonizing the study pool were sampled daily and Zooplankton sampling was carried out at weekly intervals. From early October until the pool dried in June, 1365 sticklebacks entered and only 139 stickleback's fry and seven adults left the pool. Zooplankton abundance was high during the whole study period with a mean density of 1360 ind. 100cm^?2. Larger forms (Daphnia magna, Simocephalus vetulus, Arctodiaptomus wierzejskii) quickly disappeared after the first wave of sticklebacks entered the pool in November. Subsequently, smaller species (Diacyclops bicuspidatus odessanus, Chydorus sphaericus and ostracods) replaced the larger ones until the pool dried.
• 3 Food selectivity of sticklebacks and daily Zooplankton consumption were investigated under experimental conditions within the pool in spring. After introduction of sticklebacks, densities of Zooplankton species dropped quickly (D. b. odessanus, C. sphaericus) with the exception of Ostracoda. Estimates of daily Zooplankton consumption by adult sticklebacks varied between 2.8 and 10.7% of fish body weight. Examination of gut contents showed that fry mainly ingested Chydorus sphaericus.
• 4 Given that the stickleback is an annual species in the Camargue, and that few fry are able to leave the pool due to the early drying out, the colonization of such a former fish-free pool is not beneficial for the stickleback population. However, a more serious effect of such colonization is the progressive local extinction of the most typical Zooplankton species inhabiting these formerly fish-free environments.

     

Factors affecting mate desertion by males in free-ranging convict cichlids (Cichlasoma nigrofasciatum)

Convict cichlid fish have biparental care for a period of about6 weeks lasting from egg laying until the young (fry) have grownto about 10 mm. However, the young can sometimes survive withcare from only one parent, and desertion of the mate and offspringby males has been observed. I tested a theoretical model modifiedfrom Lazarus (1990) which predicted that mate and offspringdesertion by male convict cichlids should be promoted by lowpredation pressure on fry, high remating opportunities for males,increasing age of fry, and decreasing number of fry. Males deserted7.8% of 334 broods studied during two breeding seasons in CostaRican streams. As predicted, males deserted their broods mostfrequently at sites with the highest brood survivorship (lowestbrood predation pressure), when fry were close to independenceand when brood size was smaller than average. Sex ratios andinterspawning intervals did not indicate any relationship betweenmate desertion and opportunities for remating for males. Thereuse of spawning caves may favor fidelity to the mate and brood,and defending the young from predators at the same time as defendingthe cave from conspecifics may favor biparental care in thisspecies.     

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.