The influence of ambient ultraviolet light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus)

Exposure to enhanced levels of ambient ultraviolet (UV) radiation (UVR) can have adverse effects on aquatic organisms including damage at the cellular and molecular level and impairment of development, fecundity and survival. Much research has been conducted on the role of the harmful UVB radiation. However, due to its greater penetration in water the more abundant UVA radiation can also act as an environmental stressor. Little is known about UVR effects on sperm characteristics although sperm cells should be especially prone to UV-induced oxidative stress. Moreover, UV-related changes in oxidative status may affect the phenotypic expression of energetically costly sexual ornaments. We investigated the effects of long-term exposure to ecologically relevant levels of simulated UVA radiation on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Males were assigned to three spectral exposure treatments differing in the UV spectral part so that they received either enhanced, moderate or no UVA radiation. The results reveal that exposure to enhanced ambient UVA levels had detrimental effects on both male breeding coloration and sperm velocity providing evidence that UVR affects traits targeted by pre- and post-copulatory sexual selection. By highlighting the role of UVA as a factor influencing fitness-relevant traits, our findings may contribute to a better understanding of the consequences of current and future levels of solar UVR for mating systems and life history.     

Compensatory growth response in three-spined stickleback in relation to feed-deprivation protocols

Different protocols of food deprivation were used to bring two groups of juvenile three-spined sticklebacks Gasterosteus aculeatus to the same reduced body mass in comparison with a control group fed daily ad libitum . One group experienced 1 week of deprivation then 2 weeks on maintenance rations. The second group experienced 1 week of ad libitum feeding followed by 2 weeks of deprivation. The deprived groups were reduced to a mean mass of c . 80% of controls. The compensatory growth response shown when ad libitum feeding was resumed was independent of the trajectory by which the three-spined sticklebacks had reached the reduced body mass. The compensatory response was sufficient to return the deprived groups to the mass and length trajectories shown by the control group within 4 weeks. There was full compensation for dry mass and total lipid, but incomplete compensation for lipid-free dry mass. Hyperphagia and increased growth efficiency were present in the re-feeding phase, but there was a lag of a week before the hyperphagia was established. The consistency of the compensatory response of immature three-spined sticklebacks provides a potential model system for the analysis and prediction of appetite and growth in teleosts.     

Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks

Proteins of the major histocompatibility complex (MHC) play a central role in the presentation of antigens to the adaptive immune system. The MHC also influences the odour-based choice of mates in humans and several animal taxa. It has recently been shown that female three-spined sticklebacks (Gasterosteus aculeatus) aim at a moderately high MHC diversity in their offspring when choosing a mate. Do they optimize the immune systems of their offspring? Using three-spined sticklebacks that varied in their individual numbers of MHC class IIB molecules, we tested, experimentally, whether allelic diversity at the MHC influences parasite resistance and immune parameters. We found that sticklebacks with low MHC diversity suffered more from parasite infection after experimental exposure to Schistocephalus solidus tapeworms and Glugea anomala microsporidians. They also showed the highest proportion of granulocytes and the strongest respiratory burst reaction, which are correlates of innate immunity. This indicates a strong activity of the innate immune system after challenge by parasites when MHC diversity is suboptimal. Individuals with very high allelic diversity at the MHC seemed inferior to those with moderately high diversity. Such a pattern is consistent with theoretical expectations of an optimal balance between the number of recognizable antigens and self-tolerance.     

Experimental examination of the effects of ultraviolet-B radiation in combination with other stressors on frog larvae

Ultraviolet-B radiation (UVB) is a ubiquitous stressor with negative effects on many aquatic organisms. In amphibians, ambient levels of UVB can result in impaired growth, slowed development, malformations, altered behavior and mortality. UVB can also interact with other environmental stressors to amplify these negative effects on individuals. In outdoor mesocosm and laboratory experiments we studied potential synergistic effects of UVB, a pathogenic fungus, Batrachochytrium dendrobatidis (Bd), and varying temperatures on larval Cascades frogs (Rana cascadae). First, we compared survivorship, growth and development in two mesocosm experiments with UVB- and Bd-exposure treatments. We then investigated the effects of UVB on larvae in the laboratory under two temperature regimes, monitoring survival and behavior. We found reduced survival of R. cascadae larvae with exposure to UVB radiation in all experiments. In the mesocosm experiments, growth and development were not affected in either treatment, and no effect of Bd was found. In the laboratory experiment, larvae exposed to UVB demonstrated decreased activity levels. We also found a trend towards reduced survival when UVB and cold temperatures were combined. Our results show that amphibian larvae can suffer both lethal and sublethal effects when exposed to UVB radiation.     

Physiological effects in juvenile three-spined sticklebacks feeding on toxic cyanobacterium Nodularia spumigena-exposed zooplankton

Feeding rate, growth and nutritional condition as well as nodularin concentration of juvenile three-spined sticklebacks Gasterosteus aculeatus were assessed in an experimental study where field-collected fish were given a diet of zooplankton fed with toxic Nodularia spumigena for 15 days. Food consumption was higher in N. spumigena bloom conditions compared with the cyanobacterium-free control, but despite this the growth rate of exposed fish did not improve. Control fish and fish fed N. spumigena -exposed zooplankton had higher RNA:DNA ratios and protein content than fish grown in cyanobacterial bloom conditions indicating good nutritional condition and recent growth of fish, whereas in bloom conditions metabolic transformation of nodularin to less toxic compounds may cause an energetic cost to the fish affecting the growth rate of the whole organism. Juvenile three-spined sticklebacks collected from the field contained higher concentrations of nodularin at the beginning of the experiment (mean 503·1 μg kg⁻¹). After 15 days, the lowest nodularin concentrations in fish were measured in the control treatment, suggesting that fish fed with non-toxic food are able to detoxify nodularin from their tissues more effectively than fish in continuing exposure.     

Additive effects of enhanced ambient ultraviolet B radiation and increased temperature on immune function, growth and physiological condition of juvenile (parr) Atlantic Salmon, Salmo salar

Climate change models predict increased ultraviolet B (UVB) radiation levels due to stratospheric ozone depletion and global warming. In order to study the impact of these two environmental stressors acting simultaneously on the physiology of fish, Atlantic salmon parr were exposed, for 8 weeks in outdoor tanks, to different combinations of UVB radiation (depleted and enhanced) and temperature (standard rearing temperature of 14 °C or 19 °C). The immune function (plasma IgM, lysozyme activity and complement bacteriolytic activity), growth (body weight) and physiological condition (haematocrit and plasma protein concentration) of the fish were determined. Increased UVB level, regardless of water temperature, had a negative effect on immune function parameters, growth and physiological condition. Higher temperature increased plasma IgM concentration but had a negative effect on complement bacteriolytic activity under both spectral treatments. Increased temperature, irrespective of UVB level, increased fish growth but negatively affected haematocrit and plasma protein. Exposing the fish to enhanced UVB at elevated temperature increased plasma IgM concentration and slightly improved growth. However, complement activity and physiological condition parameters decreased more than when the fish were exposed to each stressor separately. The changes were mainly additive; no interactive or synergistic effects were observed. The negative impact of multiple stressors on immune function, together with predicted increases in pathogen load in warmer waters resulting from global climate change, suggest an increased risk to diseases in fishes.     

Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks

Optimal life-history models generally predict that the reproductive effort of iteroparous organisms may increase with age, as their expectation of future reproduction decreases. The population of three-spined sticklebacks (Gasterosteus aculeatus) in the Camargue (Rhone River Delta, France) is annual, all adults dying after their first breeding season. As the three-spined stickleback is a multiple spawner, we tested the hypothesis that reproductive effort may increase during the breeding season on field data. From 1987 to 1998, 653 female sticklebacks were collected in the field during the breeding seasons. The body size, body weight and weights of the liver, gonads and carcass were measured for these individuals. Only gravid females with mature eggs (176 fish) were included in the analysis. Considering the female three-spined stickleback as a capital breeder, the energetic resources available for allocation between soma and gonads were estimated by its body weight. Somatic condition decreased during the breeding season and reproductive effort (gonad weight relative to body weight) increased. These patterns did not vary significantly between years. These observed variations in reproductive effort during the breeding season can be interpreted as empirical evidence of a trade-off between reproductive effort and expectation of future reproduction.     

Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta-analysis

Ultraviolet-B (UVB) radiation is a global stressor with potentially far-reaching ecological impacts. In the first quantitative analysis of the effects of UVB on aquatic organisms, we used meta-analytic techniques to explore the effects of UVB on survival and growth in freshwater and marine systems. Based on the large body of literature on the effects of UVB in aquatic systems, we predicted that UVB would have different effects in different habitats, experimental venues, trophic groups and life history stages. Contrary to our predictions, we found an overall negative effect of UVB on both survival and growth that crossed life histories, trophic groups, habitats and experimental venues. UVB had larger negative effects on growth in embryos compared with later life history stages. Despite the overall negative effect of UVB, effect sizes varied widely. In the survival analyses, no relationship between mean effect size and taxonomic groups or levels of exposure to UVB was detected. In the growth analyses, a larger negative effect on protozoans was observed. Our analyses suggest that the effects of UVB in aquatic systems are large and negative but highly variable between organisms. Variation in susceptibility may have important implications for population and community structure.     

Impacts of enhanced UVB radiation on photosynthetic characteristics of the marine diatom <Emphasis Type="Italic">Phaeodactylum tricornutum</Emphasis> (Bacillariophyceae,Heterokontophyta)

Solar ultraviolet B (UVB) irradiance at the Earth’s surface is increasing due to anthropogenic influences. To evaluate the effects of enhanced UVB radiation on photosynthetic characteristics of the marine diatom Phaeodactylum tricornutum, the species was exposed to four levels of UVB radiation, 0, 0.25, 0.75, and 1.50 KJ m^?2 day^?1 for 7 days. Effects of UVB stress on net photosynthetic rate, net respiration rate, variable chlorophyll (Chl) fluorescence parameters, Chl a and carotenoid contents, and UV-absorbing compounds (UVACs) were investigated. Results showed that there were no significant differences in terms of net respiration rate or maximal photochemical efficiency of photosystem II (F_v/F_m) between the treatments in the short or long term. However, enhanced UVB radiation at an intensity of 0.16 W m^?2 had a negative effect on the net photosynthetic rate, electron transport rate, and on the pathway of excess energy dissipation over the short term (1 to 5 days). Carotenoid and UVACs content increased under UVB radiation. Photosynthetic parameters were unaffected by UVB radiation on the seventh day indicating that P. tricornutum can adapt to UVB radiation in the long term. Results of the present study indicate that there is a dynamic balance between damage and adaptation in microalgae that enables them to adapt to UVB-induced photosystem alterations during both short-term and long-term exposure.     

Acid stress increases pelvic spine asymmetry in juvenile three-spined sticklebacks

In the evaluation of the effect of acidic water on the symmetrical development of the pelvic spines in juvenile three-spined sticklebacks Gasterosteus aculeatus , directional rather than fluctuating asymmetry was found, with left spines being, on average, longer than the right. Fish that were exposed for a period of c. 2 months to acidic pH levels grew significantly more asymmetrical pelvic spines than their control full-siblings held in unmanipulated water. Average spine size was not affected by the experimental treatment.     

Spiggin levels are reduced in male sticklebacks infected with Schistocephalus solidus

Using an enzyme-linked immunosorbent assay (ELISA) based technique, Schistocephalus solidus infection was shown to considerably reduce levels of spiggin in the kidney of male three-spined sticklebacks Gasterosteus aculeatus from an oligotrophic upland lake. These results suggested a graduated effect of the infection on the reproductive physiology of male three-spined sticklebacks.     

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.     

Condition factor and hepatosomatic index as estimates of energy status in male three-spined stickleback

Seasonal variation in direct and indirect measures of energy status was examined using estimates of glycogen, lipid and protein levels in a single cohort of male three-spined sticklebacks from an annual population collected each month over one complete year. Condition factor, somatic condition factor and hepatosomatic index (HSI) were calculated as indirect indices of energy status and the accuracy of these indirect measures as predictors of energy status was investigated. Results indicate that both condition factors were significant predictors of energy reserves (lipid, protein, glycogen and total energy), but that the proportion of variance accounted for was small. Both condition factors perform better as predictors of energy content per unit body weight. The HSI was a significant, but a weak predictor of total glycogen levels over the whole year. On a seasonal basis the relationship between HSI and energy reserves was highly variable. These indices are therefore poor predictors of energy reserves in male three-spined sticklebacks.     

Parasites grow larger in faster growing fish hosts

Parasites depend on host-derived energy for growth and development, and so are potentially affected by the host's ability to acquire nutrients under competitive foraging scenarios. Although parasites might be expected to grow faster in hosts that are better at acquiring nutrients from natural ecosystems, it is also possible that the most competitive hosts are better at countering infections, if they have an improved immune response or are able to limit the availability of nutrients to parasites. I first quantified the ability of uninfected three-spined sticklebacks Gasterosteus aculeatus to compete in groups for sequentially-presented food items, and then exposed either the best or worst competitors to infective stages of the cestode Schistocephalus solidus. Fish were subsequently raised in their original groups, under competitive feeding regimes, for 96 days, after which fish and parasite growth was determined. Unexpectedly, pre-exposure host competitive ability had no effect on susceptibility to infection, or on post-infection growth rate. Furthermore, despite a 120-fold variation in parasite mass at the end of the study, pre-infection competitive ability was not related to parasite growth. The closest predictor of parasite mass was body size-corrected host growth rate, indicating that the fastest growing fish developed the largest parasites. Faster growing hosts therefore apparently provide ideal environments for growing parasites. This finding has important implications for ecology and aquaculture.     

Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water?

Although the sperm of externally fertilizing fishes usually has a brief life span of up to a few minutes, this study showed that the sperm of the three-spined stickleback Gasterosteus aculeatus moved for several hours in brackish water and up to at least 10 h in the presence of ovarian fluid. Three-spined sticklebacks were able to spawn in waters ranging from full-strength sea water to fresh water, an ability unusual among fishes. The influence of salinity on sperm motility was examined, using three-spined sticklebacks from sea (salinity 30), brackish (5·5) and freshwater (0) populations. All three populations were found to have sperm with long motility periods in brackish water, lasting 165–270 min. Seawater three-spined sticklebacks had sperm motile for up to 65 min in sea water, whereas sperm from fresh- and brackish-water fish were quiescent in this medium. In fresh water, sperm from all three populations showed a very brief motility period, lasting <60 s. The presence of ovarian fluid, however, prolonged the motility period of sperm from both fresh- and brackish-water three-spined sticklebacks, for up to 7 and 10 h in fresh and brackish water, respectively, with some sperm found to be motile for up to 24 h. The results indicated that ovarian fluid created a favourable environment for the sperm and might have facilitated the three-spined sticklebacks' successful penetration of fresh water.     

Clone-specific responses in leaf phenolics of willows exposed to enhanced UVB radiation and drought stress

The effects of enhanced UVB radiation and drought stress on willow secondary phenolics were studied using the leaves of 8‐week‐old micropropagated plantlets from interspecific hybrids (Salix myrsinites L. ×S. myrsinifolia Salisb.) and pure species (S. myrsinifolia). The plantlets were subjected for 4 weeks to two levels of UVB radiation (ambient, enhanced) and two levels of watering (well‐watered, drought‐stressed) according to a 2 × 2 factorial design. Enhanced UVB radiation increased the total concentration of flavonoids and phenolic acids in all plantlets, while the total concentration of salicylates remained unaffected. Drought stress reduced the total concentration of salicylates and phenolic acids in S. myrsinifolia plantlets, while in hybrids only phenolic acids were affected. The response of phenolic acids to enhanced UVB in drought‐stressed plantlets was different from that in well‐watered ones, indicating that drought stress limited the accumulation of phenolic acids under enhanced UVB radiation. Flavonoids increased in response to enhanced UVB radiation in drought‐stressed plantlets, although drought caused serious physiological stress on growth. There were significant differences between hybrid and S. myrsinifolia plantlets with respect to the composition of phenolics and between families and clones with respect to their concentration. In addition, the response of salicylates, flavonoids and phenolic acids to enhanced UVB and drought stress was clone‐specific, which may indicate that climatic changes will alter the genetic composition of northern forests.     

Variation in Age and Size in Fennoscandian Three-Spined Sticklebacks (Gasterosteus aculeatus)

Average age and maximum life span of breeding adult three-spined sticklebacks (Gasterosteus aculeatus) were determined in eight Fennoscandian localities with the aid of skeletochronology. The average age varied from 1.8 to 3.6 years, and maximum life span from three to six years depending on the locality. On average, fish from marine populations were significantly older than those from freshwater populations, but variation within habitat types was large. We also found significant differences in mean body size among different habitat types and populations, but only the population differences remained significant after accounting for variation due to age effects. These results show that generation length and longevity in three-spined sticklebacks can vary significantly from one locality to another, and that population differences in mean body size cannot be explained as a simple consequence of differences in population age structure. We also describe a nanistic population from northern Finland exhibiting long life span and small body size.     

The effect of size of food ration on egg production in the female three-spined stickleback, Gasterosteus aculeatus L.

The effect of food level on the egg production of three-spined sticklebacks was studied experimentally. High food levels increased the percentage of fish that matured, and the weight of the fish at maturity. Weight at maturity was positively correlated with the number of spawnings, the mean number and the weight of eggs produced per spawning. Food level had no effect on the size of the eggs, whether size was expressed as wet or dry weight per egg. Fish on the highest food level spawned at shorter intervals than fish at the lower levels. A preliminary model of the effect of food supply on recruitment to a stickleback population is nresented.     

MHC genes and oxidative stress in sticklebacks: an immuno-ecological approach

Individual variation in the susceptibility to infection may result from the varying ability of hosts to specifically recognize different parasite strains. Alternatively, there could be individual host differences in fitness costs of immune defence. Although, these two explanations are not mutually exclusive, they have so far been treated in separate experimental approaches. To analyse potential relationships, we studied body condition and oxidative stress, which may reflect costs of immunity, in three-spined sticklebacks that had been experimentally exposed to three species of naturally occurring parasite. These sticklebacks differed in a trait, which is crucial to specific parasite defence, i.e. individual genetic diversity at major histocompatibility complex (MHC) class IIB loci. Oxidative stress was quantified as tissue acrolein, a technique that has been applied to questions of immuno-ecology for the first time. We measured gene expression at the MHC and other estimates of immune activation. We found that fish with high levels of MHC expression had poor condition and elevated oxidative stress. These results indicate that MHC-based specific immunity is connected with oxidative stress. They could, thus, also be relevant in the broader context of the evolution of sexually selected signals that are based on carotenoids and are, thus supposed to reflect oxidative stress resistance.