Population genetic dynamics of three-spined sticklebacks (Gasterosteus aculeatus) in anthropogenic altered habitats

In industrialized and/or agriculturally used landscapes, inhabiting species are exposed to a variety of anthropogenic changes in their environments. Genetic diversity may be reduced if populations encounter founder events, bottlenecks, or isolation. Conversely, genetic diversity may increase if populations adapt to changes in selective regimes in newly created habitats. With the present study, genetic variability of 918 sticklebacks from 43 samplings (21.3 ± 3.8 per sample) at 36 locations from cultivated landscapes in Northwest Germany was analyzed at nine neutral microsatellite loci. To test if differentiation is influenced by habitat alterations, sticklebacks were collected from ancient running waters and adjacent artificial stagnant waters, from brooks with salt water inflow of anthropogenic and natural origin and adjacent freshwater sites. Overall population structure was dominated by isolation by distance (IBD), which was significant across all populations, and analysis of molecular variance (AMOVA) revealed that 10.6% of the variation was explained by river catchment area. Populations in anthropogenic modified habitats deviated from the general IBD structure and in the AMOVA, grouping by habitat type running/stagnant water explained 4.9% of variation and 1.4% of the variation was explained by salt-/freshwater habitat. Sticklebacks in salt-polluted water systems seem to exhibit elevated migratory activity between fresh- and saltwater habitats, reducing IBD. In other situations, populations showed distinct signs of genetic isolation, which in some locations was attributed to mechanical migration barriers, but in others to potential anthropogenic induced bottleneck or founder effects. The present study shows that anthropogenic habitat alterations may have diverse effects on the population genetic structure of inhabiting species. Depending on the type of habitat change, increased genetic differentiation, diversification, or isolation are possible consequences.     

Interplay of individual interactions and turbidity affects the functional response of three-spined sticklebacks Gasterosteus aculeatus

The effects of turbidity, size and the presence of conspecifics on the functional response, feeding latency and activity in the three-spined stickleback Gasterosteus aculeatus were examined. A significant interaction between standard length and presence of conspecifics demonstrated an increase in attack rates of larger individuals in the presence of conspecifics. Attack rate was also higher in turbid water. Feeding latency decreased with prey concentration and presence of conspecifics, but was not affected by turbidity. Activity level did not change with prey levels, but increased with turbidity. These results can help to better understand how individual flexibility in the functional response can affect prey mortality according to environmental perturbation and social interaction at the level of the predator.     

Aging three-spined sticklebacks Gasterosteus aculeatus: comparison of estimates from three structures

In order to assess the accuracy and reliability of age estimates from calcified structures in the three-spined stickleback Gasterosteus aculeatus, we evaluated intra and inter-reader repeatability from three structures: otoliths, gill covers and pelvic spines). Average age estimates were also compared between the structures. The overall intra-reader repeatability of age estimates were highest for otoliths (69%), lowest for gill covers (53%) and intermediate for spine cross-sections (63%). Although four of the seven readers had the highest intra-reader repeatability score for spine cross-sections, the inter-reader variance in this structure was much higher than in others. Otoliths were the easiest in terms of their pre-analysis treatment and exchange of materials (as digital images) between readers. In addition, otoliths are more well-studied compared with the other structures with respect to their development through ontogenesis; hence, age estimates based on otoliths should be the most reliable. Therefore, our recommendation is that whenever possible, analysis of otoliths should be the preferred approach for aging G. aculeatus.     

Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus)

Acoustic noise is known to have a variety of detrimental effects on many animals, including humans, but surprisingly little is known about its impacts on foraging behaviour, despite the obvious potential consequences for survival and reproductive success. We therefore exposed captive three-spined sticklebacks (Gasterosteus aculeatus) to brief and prolonged noise to investigate how foraging performance is affected by the addition of acoustic noise to an otherwise quiet environment. The addition of noise induced only mild fear-related behaviours--there was an increase in startle responses, but no change in the time spent freezing or hiding compared to a silent control--and thus had no significant impact on the total amount of food eaten. However, there was strong evidence that the addition of noise increased food-handling errors and reduced discrimination between food and non-food items, results that are consistent with a shift in attention. Consequently, noise resulted in decreased foraging efficiency, with more attacks needed to consume the same number of prey items. Our results suggest that acoustic noise has the potential to influence a whole host of everyday activities through effects on attention, and that even very brief noise exposure can cause functionally significant impacts, emphasising the threat posed by ever-increasing levels of anthropogenic noise in the environment.     

Experience of natural prey and feeding efficiency in three-spined sticklebacks (Gasterosteus aculeatus L.)

The possibility that efficiency of feeding on different prey in three-spined sticklebacks ( Gasterosteus aculeatus L.) increases by experience of such items was investigated experimentally by comparing sticklebacks reared with only non-moving prey (frozen brine shrimps) with sticklebacks caught in the wild from localities where a wide range of prey species was available. Fish without experience of natural food scored less well than those from the wild on various components of foraging and so had reduced feeding efficiency. However, feeding efficiency in naive fish improved after just a few days of experience with natural prey. Such experience-induced changes in foraging efficiency will alter the profitability of prey items for individual fish.     

Habitat scale, female cannibalism, and male reproductive success in three-spined sticklebacks (Gasterosteus aculeatus)

We studied the effects of habitat scale (pool size) on the riskof egg cannibalism and the breeding behavior of three-spinedsticklebacks (Gasterosteus aculeatus). Laboratory experimentsshowed that in pools with similar population density, a largerfraction of males nested in pools of 4.8-m² surface area thanin 15-m² pools. Breeding males in the 4.8-m² pools also hadbigger territories, obtained more eggs, and were more aggressivetoward intruders than those in the 15-m² pools. The numbersof raids attempted on nests were similar in the two pool sizes.However, raiding-shoal sizes were larger, and hence individualsin these larger shoals were more succesful at overwhelming maleterritorial defenses in the 15-m² pools than in the 4.8-m² pools.At the field site, a salt marsh containing hundreds of tidepools of different sizes, sticklebacks settled at similar densitiesin small (<30 m² surface area) and large (>355 m²) pools.This resulted in significantly more fish being present in largepools than in small pools, a concomitant increase in the amountof nest raiding, and a decrease in individual male reproductivesuccess in large compared to small pools. A photogrammetry analysisof the salt-marsh pools suggests that the majority of fish breedingat the site will be subjected to a high risk of cannibalismbecause most fish nest in large pools. We conclude that spatialscale has a major influence on this species' breeding behaviorand reproductive success.     

The influence of hunger on shoal size choice by three-spined sticklebacks, Gasterosteus aculeatus

Single sticklebacks ( Gasterosteus aculeatus ) were presented with a choice between (a) a shoal and an empty compartment, and (b) two different sized shoals of conspecifics. The choice of hungry test fish (food-deprived for 24 h and 72 h, respectively) was compared to that of fish which were fed to satiation once a day. It was hypothesized that due to the increased level of competition for food in large shoals, hungry fish would spend less time with the larger of two shoals than their well-fed conspecifics. The results showed that there was indeed a significant trend for test fish to spend a decreasing amount of time near the compartment with the larger number of fish with increasing duration of food deprivation.     

Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus)

A perplexing new question that has emerged from the recent surge of interest in behavioural syndromes or animal personalities is – why do individual animals behave consistently when behavioural flexibility is advantageous? If individuals have a tendency to be generally aggressive, then a relatively aggressive individual might be overly aggressive towards offspring, mates or even predators. Despite these costs, studies in several taxa have shown that individuals that are more aggressive are also relatively bold. However, the behavioural correlation is not universal; even within a species, population comparisons have shown that boldness and aggressiveness are correlated in populations of sticklebacks that are under strong predation pressure, but not in low predation populations. Here, we provide the first demonstration that an environmental factor can induce a correlation between boldness and aggressiveness. Boldness under predation risk and aggressiveness towards a conspecific were measured before and after sticklebacks were exposed to predation by trout, which predated half the sticklebacks. Exposure to predation generated the boldness–aggressiveness behavioural correlation. The behavioural correlation was produced by both selection by predators and behavioural plasticity. These results support the hypothesis that certain correlations between behaviours might be adaptive in some environments.     

The breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigour

Summary A necessary condition of most models of intersexual selection requires that secondary sexual traits are costly so that cheating is prevented. If the conspicuous breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus L.) is such a handicap, it must involve costs. I examined the energetic costs of the breeding colouration by varying the energy contents of the daily food supply among five groups of sticklebacks over a 10 week period. The nutritional carotenoid level, i.e. the colour pigment used in the breeding colouration, was constant for all fish. Both the increase of their condition factor and the condition level they finally achieved correlated positively with the food ration of the groups. Individuals whose condition increased during the experiment developed a more intensive red colouration. However, a direct correlation between food quantity and the red breeding colouration reached at the end of the experiment did not exist. Nevertheless, given the limitation of pigment availability, there was still variation in the breeding colouration and the costs for the metabolism of the colouration were sufficient to render it an honest signal: a female stickleback can assess a male's condition and condition change over the past few weeks by the intensity of the colour of his blue eyes (which is not based on carotenoids and whose pigments were therefore not controlled in the food) and his red jaw, respectively. How much an individual male fish invests in increase of length and increase of condition (which correlate negatively with each other) seems to be, at least partly, his own strategic decision, which could have important consequences in the competition for female mates. It is eventually this decision that a male stickleback seems to signal with his red jaw.     

The influence of ambient water temperature on sperm performance and fertilization success in three-spined sticklebacks (Gasterosteus aculeatus)

Acute and long-term temperature changes caused by global warming could lead to severe ecological and physiological consequences for aquatic organisms. This might be reflected in a higher mortality rate or a reduced hatching success but elevated temperatures might also lead to accelerated growth and egg development due to higher metabolic rates. Thermal conditions could also act on male gamete function that is known to be under strong sexual selection especially in mating systems where sperm competition frequently occurs. The three-spined stickleback (Gasterosteus aculeatus) is an externally fertilizing fish species. Males are sperm limited over the course of one breeding season and the risk of sperm competition is known to be high. To study the impact of ecologically relevant water temperatures in relation to different sperm numbers on reproductive performance standardized in vitro fertilization experiments were conducted, using two different immediate temperature changes (15 and 25 °C) as all test individuals were held under the same conditions prior to the experiments. The results revealed that fertilization success differed significantly when using different sperm numbers in different water temperatures. At higher temperatures a lower number of sperm was sufficient to fertilize 50 % of the eggs. However, with increasing sperm number fertilization success saturated at 75 % in the 25 °C treatment but at about 90 % in the 15 °C treatment. A further experiment dealt with sperm swimming ability at different temperatures (5, 15 and 25 °C), showing that both sperm velocity and linearity significantly increased whereas the percentage of motile sperm decreased at higher temperatures, suggesting that under these conditions sperm might reach an unfertilized egg more rapidly but live shorter. The observed results stress the role of current and future levels of naturally occurring ambient water temperatures as an important environmental factor influencing fitness related traits.     

A comparison of nest building by three-spined sticklebacks Gasterosteus aculeatus from still and flowing waters

The composition of nests, built under standardized, static laboratory conditions by male three-spined sticklebacks Gasterosteus aculeatus from two rivers and two lakes in mid-Wales (U.K.) was quantified. After transfer to nesting tanks, fish from the rivers began building nests more quickly than fish from the lakes. The number of threads used in nest construction and the mass of substrate deposited co-varied, but there were no consistent population- or habitat-related differences in the aspects of nest composition.     

Parasites may contribute to 'magic trait' evolution in the adaptive radiation of three-spined sticklebacks, Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae)

In the past decade, there has been a new effort to understand the ecology that drives population divergence and speciation. It is well established in theory that speciation is most likely to occur when a trait that is under divergent natural selection in different populations is also used in mate choice. Such traits have been dubbed 'magic traits' ( Gavrilets, 2004 ) and, although there appears to be good evidence that they exist, the ecological mechanisms that underlie their divergence are not well understood. Size at maturity in three-spined sticklebacks is an archetypal example of a magic trait. The present study documents for the first time that differences in body size at maturity in sympatric species pairs of lacustrine three-spined sticklebacks in British Columbia, Canada, are caused by differences in age at maturity. It is also shown that there are differences between the sympatric species in the patterns of infection with a virulent cestode, Schistocephalus solidus . Although the evidence is circumstantial, these differences in infection are consistent with the hypothesis that they have contributed to the observed divergence in age and size at maturity in these populations.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 425–433.     

Inheritance of vertebral number in the three-spined stickleback (Gasterosteus aculeatus)

Intraspecific variation in the number of vertebrae is taxonomically widespread, and both genetic and environmental factors are known to contribute to this variation. However, the relative importance of genetic versus environmental influences on variation in vertebral number has seldom been investigated with study designs that minimize bias due to non-additive genetic and maternal influences. We used a paternal half-sib design and animal model analysis to estimate heritability and causal components of variance in vertebral number in three-spined sticklebacks (Gasterosteus aculeatus). We found that both the number of vertebrae (h² = 0.36) and body size (h² = 0.42) were moderately heritable, whereas the influence of maternal effects was estimated to be negligible. While the number of vertebrae had a positive effect on body size, no evidence for a genetic correlation between body size and vertebral number was detected. However, there was a significant positive environmental correlation between these two traits. Our results support the generalization-in accordance with results from a review of heritability estimates for vertebral number in fish, reptiles and mammals-that the number of vertebrae appears to be moderately to highly heritable in a wide array of species. In the case of the three-spined stickleback, independent evolution of body size and number of vertebrae should be possible given the low genetic correlation between the two traits.     

Indices of stress in three-spined sticklebacks Gasterosteus aculeatus in relation to extreme weather events and exposure to wastewater effluent

Whole-body concentrations of cortisol and glucose were measured in three-spined sticklebacks Gasterosteus aculeatus from two rivers (Rivers Ray and Ock) in southern England during a 30 month period in order to assess effects on the stress axis of (1) remediation of a wastewater treatment works (WWTW) effluent (River Ray) and (2) episodic changes in flow rate arising from periods of high rainfall (Rivers Ray and Ock). The postcapture concentrations of cortisol and glucose in fish from both rivers did not exhibit a seasonal periodicity but did show significant between-sample, between-site and between-river variation, superimposed upon a consistent downward trend for each analyte during the monitoring period. Corticosteroid and glucose concentrations following capture were inversely linked with a progressive increase in condition of the fish during this period. Site-dependent trends possibly related to exposure to the WWTW effluent were detected for both analytes in fish from the River Ray. For fish in the River Ray, a significant proportion of variation in both corticosteroid and glucose concentrations, additional to the downward trend with time, was accounted for by temporal proximity of the sample to exceptional flow events arising from episodes of high rainfall and high turbidity. This relationship was not statistically significant for fish from the River Ock. These data suggest that the responsiveness of the stress axis in free-living G. aculeatus may be altered by exposure to WWTW effluent and by exposure to physical changes in the aquatic environment such as those arising from extreme weather events. The magnitude of these effects may be increased by exposure to both stressors concurrently.     

Water temperature,not fish morph,determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)

Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the host environment. It is possible that different morphs experience specific selection gradients by parasites but it is not clear how consistent the selection is when abiotic factors change. We examined parasite pressure in sympatric morphs of threespine stickleback (Gasterosteus aculeatus) across a temperature gradient in two large Icelandic lakes, Myvatn and Thingvallavatn. Habitat‐specific temperature gradients in these lakes are opposite. Myvatn lava rock morph lives in a warm environment, while the mud morph lives in the cold. In Thingvallavatn, the lava rock morph lives in a cold environment and the mud morph in a warm habitat. We found more parasites in fish living in higher temperature in both lakes, independent of the fish morph, and this pattern was similar for the two dominating parasite taxa, trematodes and cestodes. However, at the same time, we also found higher parasite abundance in a third morph living in deep cold–water habitat in Thingvallavatn compared to the cold‐water lava morph, indicating strong effect of habitat‐specific biotic factors. Our results suggest complex interactions between water temperature and biotic factors in determining the parasite community structure, a pattern that may have implications for differentiation of stickleback morphs.