Invertebrate studies at S'Albufera Natural Park

Work was begun in spring 1989 to obtain en inventory of invertebrates present in the Park, to investigate the composition of invertebrate fauna in relation to habitat and to physical and seasonal variables, and to establish methodology designed to evaluate long-term changes in numbers and species compositions. Groups chosen for study were arachnids, Coleoptera, Lepidoptera, Odonata and freshwater invertebrates, syrphids (Oiptera) and terrestrial molluscs. The work was part of Project S'Albufera, a monitoring programme for long-term environmental change, organised by Earthwatch Europe.El treball va començar la primavera de 1989 amb l'objectiu, per una banda, d'inventariar els invertebrats presents en el Parc, investigar la composició de la fauna d'invertebrats en relació a l'hàbitat i a les variables físiques, així com la seva estacionalitat; per altra banda establir un disseny metodològic per a avaluar canvis de llarg termini en el nombre i composició d'espècies. Els grups elegits per a l'estudi foren aràcnids, coleòpters, lepidòpters, odonats i invertebrats d'aigua dolça, sírfids (Oiptera) i mol·luscs terrestres. El treball forma part del Project S'Albufera, un programa de seguiment de llarg termini del canvi ambiental organitzat per Earthwatch Europe

Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon

The risk of mortality associated with a long-distance migration will depend on an animal's physiological state, as well as the prevailing ecological conditions. Here we assess whether juvenile telomere length, which in endotherms has been shown to be a biomarker of physiological state and expected lifespan, predicts whether wild Atlantic salmon Salmo salar successfully complete their marine migration. Over 1800 juvenile fish were trapped, measured, PIT-tagged and a tissue biopsy taken when migrating as juveniles down-river towards the sea. Survivors of the marine phase of the life cycle were then re-trapped and re-sampled when returning to the river to spawn as sexually mature adults, 1.5-2.5 years later. Most individuals experienced a reduction in telomere length during the marine migratory phase of their life cycle. While the relative rate of telomere loss was greater in males than females, telomere loss was unrelated to growth at sea. Contrary to expectations, salmon that had the shortest telomeres at the time of the outward migration had the greatest probability of surviving through to the return migration. This effect, independent of body size, may indicate a trade-off between investment in readiness for marine life (which favours high glucocorticoid levels, known to increase telomere attrition in other vertebrate species) and investment in telomere maintenance. Survival was also significantly influenced by the seasonal timing of outward migration, with the fish migrating downstream earliest in the spring having the highest probability of return. This study reveals that telomere length is associated with survival, although in ways that contrast with patterns seen in endotherms. This illustrates that while telomeres may be universally important for chromosome protection, the potential for telomere dynamics to predict performance may vary across taxa

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self-evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e. telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, though the effects of other parental contribution pathways have been far less studied. By using wild Atlantic salmon with different parental life histories in an experimental split-brood IVF mating design and rearing the resulting families under standardised conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life

Maternal age at maturation underpins contrasting behaviour in offspring

In species where parental care occurs primarily via the provisioning of eggs, older females tend to produce larger offspring that have better fitness prospects. Remarkably however, a relationship between age of mother and fitness of offspring has also been reported independently of effects on offspring size suggesting that there may be other factors at play. Here, using experimental matings between wild Atlantic salmon that differed in their age at sexual maturation, we demonstrate distinct size-independent variation in the behaviour of their offspring that was related to the maturation age of the mother (but not the father). We found that when juvenile salmon were competing for feeding territories, offspring of early-maturing mothers were more aggressive than those of late-maturing mothers, but were out-competed for food by them. This is the first demonstration of a link between natural variation in parental age at maturation and variation in offspring behaviou

Adaptive maternal investment in the wild? Links between maternal growth trajectory and offspring size, growth, and survival in contrasting environments

Life history theory predicts that investment per offspring should correlate negatively with the quality of environment offspring are anticipated to encounter; parents may use their own experience as juveniles to predict this environment and may modulate offspring traits such as growth capacity as well as initial size. We manipulated nutrient levels in the juvenile habitat of wild Atlantic salmon Salmo salar to investigate the hypothesis that the egg size maximizing juvenile growth and survival depends on environmental quality. We also tested whether offspring traits were related to parental growth trajectory. Mothers that grew fast when young produced more, smaller offspring than mothers that had grown slowly to reach the same size. Despite their size disadvantage, offspring of faster-growing mothers grew faster than those of slow-growing mothers in all environments, counter to the expectation that they would be competitively disadvantaged. However, they had lower relative survival in environments where the density of older predatory/competitor fish was relatively high. These links between maternal (but not paternal) growth trajectory and offspring survival rate were independent of egg size, underscoring that mothers may be adjusting egg traits other than size to suit the anticipated environment faced by their offspring

Telomere elongation during early development is independent of environmental temperatures in Atlantic salmon

There is increasing evidence from endothermic vertebrates that telomeres, which cap the ends of chromosomes and play an important role in chromosome protection, decline in length during postnatal life and are a useful indicator of physiological state and expected lifespan. However, much less is currently known about telomere dynamics in ectothermic vertebrates, which are likely to differ from that of endotherms, at least in part due to the sensitivity of ectotherm physiology to environmental temperature. We report here on an experiment in which Atlantic salmon were reared through the embryonic and larval stages of development, and under differing temperatures, in order to examine the effects of environmental temperature during early life on telomere dynamics, oxidative DNA damage and cellular proliferation. Telomere length significantly increased between the embryonic and larval stages of development. Contrary to our expectations, variation in telomere length at the end of the larval stage was unrelated to either cell proliferation rate or the relative level of oxidative DNA damage, and did not vary between the temperature treatments. This study suggests that salmon are able to restore the length of their telomeres during early development, which may possibly help to buffer potentially harmful environmental effects experienced in early life

Habitat restoration weakens negative environmental effects on telomere dynamics

Habitat quality can have far-reaching effects on organismal fitness, an issue of concern given the current scale of habitat degradation. Many temperate upland streams have reduced nutrient levels due to human activity. Nutrient restoration confers benefits in terms of invertebrate food availability and subsequent fish growth rates. Here we test whether these mitigation measures also affect the rate of cellular ageing of the fish, measured in terms of the telomeres that cap the ends of eukaryotic chromosomes. We equally distributed Atlantic salmon eggs from the same 30 focal families into 10 human-impacted oligotrophic streams in northern Scotland. Nutrient levels in five of the streams were restored by simulating the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period, while five reference streams were left as controls. Telomere lengths and expression of the telomerase reverse transcriptase (TERT) gene that may act to lengthen telomeres were then measured in the young fish when 15 months old. While TERT expression was unrelated to any of the measured variables, telomere lengths were shorter in salmon living at higher densities and in areas with a lower availability of the preferred substrate (cobbles and boulders). However, the adverse effects of these habitat features were much reduced in the streams receiving nutrients. These results suggest that adverse environmental pressures are weakened when nutrients are restored, presumably because the resulting increase in food supply reduces levels of both competition and stress

Simulating nutrient release from parental carcasses increases the growth, biomass and genetic diversity of juvenile Atlantic salmon

The net transport of nutrients by migratory fish from oceans to inland spawning areas has decreased due to population declines and migration barriers. Restoration of nutrients to increasingly oligotrophic upland streams (that were historically salmon spawning areas) have shown short‐term benefits for juvenile salmon, but the longer term consequences are little known. Here we simulated the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period in five Scottish upland streams (‘high parental nutrient’ treatment), while leaving five reference streams without carcasses (‘low parental nutrient’ treatment). All streams received exactly the same number of salmon eggs (n = 3,000) drawn in equal number from the same 30 wild‐origin families, thereby controlling for initial egg density and genetic composition. We then monitored the resulting juvenile salmon and their macroinvertebrate prey, repeating the carcass addition treatment in the next spawning season. Macroinvertebrate biomass and abundance were five times higher in the high parental nutrient streams, even 1 year after the carcass addition, and led to faster growth of juvenile salmon over the next 2 years (but with no change in population density). This faster growth led to more fish exceeding the size threshold that would trigger emigration to sea at 2 rather than 3 years of age. There was also higher genetic diversity among surviving salmon in high parental nutrient streams; genotyping showed that these effects were not due to immigration but to differential survival. Synthesis and applications. This 2‐year field experiment shows that adding nutrients that simulate the presence of small numbers of adult salmon carcasses can have long‐term effects on the growth rate of juvenile salmon, likely increasing the number that will migrate to sea early and also increasing their genetic diversity. However, the feasibility of adding nutrients to spawning streams as a management tool to boost salmon populations will depend on whether the benefits at this stage are maintained over the entire life cycle

Simulating nutrient release from parental carcasses increases the growth, biomass and genetic diversity of juvenile Atlantic salmon

The net transport of nutrients by migratory fish from oceans to inland spawning areas has decreased due to population declines and migration barriers. Restoration of nutrients to increasingly oligotrophic upland streams (that were historically salmon spawning areas) have shown short‐term benefits for juvenile salmon, but the longer term consequences are little known. Here we simulated the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period in five Scottish upland streams (‘high parental nutrient’ treatment), while leaving five reference streams without carcasses (‘low parental nutrient’ treatment). All streams received exactly the same number of salmon eggs (n = 3,000) drawn in equal number from the same 30 wild‐origin families, thereby controlling for initial egg density and genetic composition. We then monitored the resulting juvenile salmon and their macroinvertebrate prey, repeating the carcass addition treatment in the next spawning season. Macroinvertebrate biomass and abundance were five times higher in the high parental nutrient streams, even 1 year after the carcass addition, and led to faster growth of juvenile salmon over the next 2 years (but with no change in population density). This faster growth led to more fish exceeding the size threshold that would trigger emigration to sea at 2 rather than 3 years of age. There was also higher genetic diversity among surviving salmon in high parental nutrient streams; genotyping showed that these effects were not due to immigration but to differential survival. Synthesis and applications. This 2‐year field experiment shows that adding nutrients that simulate the presence of small numbers of adult salmon carcasses can have long‐term effects on the growth rate of juvenile salmon, likely increasing the number that will migrate to sea early and also increasing their genetic diversity. However, the feasibility of adding nutrients to spawning streams as a management tool to boost salmon populations will depend on whether the benefits at this stage are maintained over the entire life cycle

Counterintuitive active directional swimming behaviour by Atlantic salmon during seaward migration in the coastal zone

Acknowledgements We thank the Cromarty Firth District Salmon Fishery Board for logistical support and three anonymous referees who improved an earlier draft of this paper. Funding for this work came from Scottish & Southern Energy Renewables. We are grateful for the skills and expertise of Bill Ruck at Moray First Marine along with the crews of Marine Scotland Science vessels who were integral to the successful deployment and recovery of equipment. Some receivers were also made available from the Ocean Tracking Network (OTN) The data underlying this article will be shared on reasonable request to the corresponding author.Peer reviewedPublisher PD