Trophic state and its implications for natural reproduction of salmonid fish

Natural propagation of all fish species native to a particular lake is an ecological requirement of prime importance. Salmonid fish are particularly vulnerable to environmental degradation since egg development takes place on or in the bottom substrate. Dissolved oxygen concentration on the spawning site is commonly considered the main factor limiting egg development. In order to assess the relationship between trophic state, hypolimnetic oxygen concentration, and salmonid egg development, whitefish (Coregonus sp.) eggs were sampled just prior to hatching in late winter. Eggs were collected in 13 Swiss lakes of different trophic state, using a sled-dredge. The proportion of viable eggs among the total number of eggs found was taken as a measure of reproductive success. The results indicate that successful in situ embryogenesis is not primarily governed by hypolimnetic oxygen concentration which tends to be high anyway during egg incubation, but by trophic state in terms of total phosphorus concentration in spring. The findings are explained by the production-related oxygen uptake of the sediment, creating an oxygen gradient of varying steepness in the diffusive boundary layer. Implications for the restoration of lacustrine ecosystems are discussed.     

Temperature extremes: geographic patterns,recent changes,and implications for organismal vulnerabilities

Extreme temperatures can injure or kill organisms and can drive evolutionary patterns. Many indices of extremes have been proposed, but few attempts have been made to establish geographic patterns of extremes and to evaluate whether they align with geographic patterns in biological vulnerability and diversity. To examine these issues, we adopt the CLIMDEX indices of thermal extremes. We compute scores for each index on a geographic grid during a baseline period (1961–1990) and separately for the recent period (1991–2010). Heat extremes (temperatures above the 90th percentile during the baseline period) have become substantially more common during the recent period, particularly in the tropics. Importantly, the various indices show weak geographic concordance, implying that organisms in different regions will face different forms of thermal stress. The magnitude of recent shifts in indices is largely uncorrelated with baseline scores in those indices, suggesting that organisms are likely to face novel thermal stresses. Organismal tolerances correlate roughly with absolute metrics (mainly for cold), but poorly with metrics defined relative to local conditions. Regions with high extreme scores do not correlate closely with regions with high species diversity, human population density, or agricultural production. Even though frequency and intensity of extreme temperature events have – and are likely to have – major impacts on organisms, the impacts are likely to be geographically and taxonomically idiosyncratic and difficult to predict.     

Environmental conditions modify density-dependent salmonid recruitment: Insights into the 2016 recruitment crash in Wales

1. Understanding the effects of density-dependent and density-independent factors on recruitment is often inhibited by difficulties quantifying their relative contributions in highly variable recruitment data. Use of data-driven statistical methods with data that include one or more extreme recruitment events could help overcome these difficulties.
2. Juvenile Atlantic salmon and trout abundances in Wales have declined over the last 2 decades, and 2016 was a notably poor recruitment year in rivers around southern Europe, including England and Wales. The 2016 recruitment crash coincided with extreme winter weather conditions, leading to speculation that unusually warm temperatures and high flows adversely affect salmonid recruitment and caused the 2016 crash, although this remains untested.
3. We developed data-driven statistical models to: (1) describe juvenile salmonid recruitment from density-dependent and density-independent factors; and (2) assess whether the density-independent factors probably contributed to the 2016 salmon recruitment crash. We compiled salmon and trout young-of-year juvenile abundances from electrofishing surveys, egg deposition estimates and river flow and air temperature data from 2001–2017 for seven Welsh rivers, broadly representative of rivers around Wales. We used river flow and air temperature data to derive ecologically and behaviourally meaningful density-independent explanatory variables.
4. Salmonid recruitment in Wales was best described using density-dependent and density-independent factors, especially for salmon: after accounting for a concave relationship with egg deposition, salmon juvenile abundance was reduced under (1) warmer spawning temperatures that might inhibit spawning, and (2) higher flood frequencies during pre-emergence and emergence that might washout eggs or alevins. Results were less clear for trout, perhaps because they are behaviourally more plastic.
5. Our findings provide empirical support for general and predictable effects of temperature and flow during spawning and emergence on salmonid—especially salmon—recruitment in Wales. Furthermore, we suggest that the 2016 salmon recruitment crash was caused—in part—by particularly inclement spawning and emergence conditions, which could be more common under future climate change. Our findings suggest that future salmonid stock assessment models could include the effects of density-independent variables on recruitment to improve their predictive power.

     

Non-climatic thermal adaptation: implications for species' responses to climate warming

There is considerable interest in understanding how ectothermic animals may physiologically and behaviourally buffer the effects of climate warming. Much less consideration is being given to how organisms might adapt to non-climatic heat sources in ways that could confound predictions for responses of species and communities to climate warming. Although adaptation to non-climatic heat sources (solar and geothermal) seems likely in some marine species, climate warming predictions for marine ectotherms are largely based on adaptation to climatically relevant heat sources (air or surface sea water temperature). Here, we show that non-climatic solar heating underlies thermal resistance adaptation in a rocky–eulittoral-fringe snail. Comparisons of the maximum temperatures of the air, the snail''s body and the rock substratum with solar irradiance and physiological performance show that the highest body temperature is primarily controlled by solar heating and re-radiation, and that the snail''s upper lethal temperature exceeds the highest climatically relevant regional air temperature by approximately 22°C. Non-climatic thermal adaptation probably features widely among marine and terrestrial ectotherms and because it could enable species to tolerate climatic rises in air temperature, it deserves more consideration in general and for inclusion into climate warming models.     

Thermal stress in Arctic charr Salvelinus alpinus broodstock: a 28 year case study

Temperature and egg viability data from an Arctic charr Salvelinus alpinus hatchery covering a period of 28 years were analysed. During the study period, there was a significant increase in the mean water temperature in May, July, August and September of c. 2° C. Independent of year, the egg viability showed a negative correlation with the mean monthly temperatures in July, August and September as well as with the temperature difference between October and November. The negative effect of high summer temperatures was further supported by a comparison of egg viability from replicate broodstock reared at two sites differing mainly in summer water temperature. The eggs from the colder site were, on average, significantly larger (4·4 mm compared with 4·0 mm) and had higher hatching rates (57% compared with 37%). These results suggest that unfavourable temperature conditions during the summer and autumn can explain much of the excessive egg mortality experienced at the main facility used for the Swedish S. alpinus breeding programme. The main effect was supra‐optimal temperatures during the period July to September, but there also appears to have been an effect from the temperature regime before and during spawning (October to November) that was unrelated to the summer temperatures. These findings emphasize the importance of site selection and sustainable management of aquaculture hatcheries in the light of the ongoing climate change.     

Competitive exclusion along climate gradients: energy efficiency influences the distribution of two salmonid fishes

We tested the importance of thermal adaptations and energy efficiency in relation to the geographical distribution of two competing freshwater salmonid fish species. Presence–absence data for Arctic char and brown trout were obtained from 1502 Norwegian lakes embracing both temperature and productivity gradients. The distributions were contrasted with laboratory‐derived temperature scaling models for food consumption, growth and energy efficiency. Thermal performances of the two species were almost identical. However, Arctic char exhibited double the growth efficiency (per unit of food) and appear to have out‐competed brown trout from cold, low‐productivity lakes, perhaps by scramble competition. Brown trout, for which previous reports have shown to be aggressive and dominant, have likely excluded the more energy‐efficient Arctic char from relatively warm, productive lakes, perhaps by contest competition. Competitive interaction changing in outcome with lake productivity, rather than thermal performance, is likely a major determinant of the range distribution of the two species. Our study highlights the need for more focus on choice of relevant ecophysiological traits in ecological climate impact studies and species distribution modelling.     

Role of colony-stimulating factor-1 in reproduction and development

The CSF-1 null mouse, osteopetrotic, has provided a powerful model in which to study the biological functions of CSF-1. In this review, I will describe our studies that have used this mouse model to determine the impact of a lack of CSF-1 on developmental processes and in reproduction. A role for CSF-1 in reproduction was originally suggested by the sex steroid hormone-regulated uterine epithelial synthesis of CSF-1 and the expression of its receptor in trophoblast and decidual cells. Studies on the fertility of CSF-1 deficient osteopetrotic mice (csfm^op/csfm^op) mice confirmed this suggestion and in addition revealed an unexpected function for CSF-1 in male fertility. In both sexes, CSF-1 appears to regulate gonadal steroidogenesis, probably through its action on macrophages that are abundant throughout the ovary and testis. In the female, CSF-1 affects ovulation in vivo and in vitro, and impacts the preimplantation embryo, increasing both its rate of development and the number of trophectodermal cells in the blastocyst. CSF-1 also has a role in mammary gland development during pregnancy, since at mid-gestation in csfm^op/csfm^op mice, ductal branching is impaired, and after partiturition, there is a failure to switch to lactation. The relative failure of csfm^op/csfm^op mice to respond to external stimuli also suggested a role for CSF-1 in the brain. CSF-1 mRNA is expressed in a regional specific manner in the brain through development whilst the CSF-1 receptor is expressed throughout the brain in microglia. CSF-1 is neurotrophic in embryonic neuronal cultures and its absence in csfm^op/csfm^op mice results in severe electrophysiological abnormalities in the cortex. This suggests that CSF-1 is a neurotrophic factor acting through the microglia. The pleiotropic roles for CSF-1 in reproduction and in the brain suggest that CSF-1 exerts many of its action through the trophic activities of cells of the mononuclear phagocytic lineage. Mol Reprod Dev 46:54–61, 1997. © 1997 Wiley-Liss, Inc.     

Low evolutionary potential for egg‐to‐adult viability in Drosophila melanogaster at high temperatures

To cope with the increasing and less‐predictable temperature forecasts under climate change, many terrestrial ectotherms will have to migrate or rely on adaptation through plastic or evolutionary means. Studies suggest that some ectotherms have a limited potential to change their upper thermal limits via evolutionary shifts, but research has mostly focused on adult life stages under laboratory conditions. Here we use replicate populations of Drosophila melanogaster and a nested half‐sib/full‐sib quantitative genetic design to estimate heritabilities and genetic variance components for egg‐to‐adult viability under both laboratory and seminatural field conditions, encompassing cold, benign, and hot temperatures in two separate populations. The results demonstrated temperature‐specific heritabilities and additive genetic variances for egg‐to‐adult viability. Heritabilities and genetic variances were higher under cold and benign compared to hot temperatures when tested under controlled laboratory conditions. Tendencies toward lower evolutionary potential at higher temperatures were also observed under seminatural conditions although the results were less clear in the field setting. Overall the results suggest that ectotherms that already experience temperatures close to their upper thermal tolerance limits have a restricted capacity to adapt to higher temperatures by evolutionary means.     

Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish

Temperature treatment of common wolffish Anarhichas lupus during vitellogenesis affected the time of final maturation; ovulation in fish held at 8 and 12° C from mid-April to October was about four and five weeks delayed, compared with a 4° C group. Fish in the 8° C group had significantly larger eggs than those in the 4° C and the 12° C groups, and a significantly higher egg production than fish in the 12° C group. Temperature treatment did not affect either fertilization rate or relative fecundity, but absolute fecundity was significantly lower in the 12° C group than the other groups due to poor growth of the fish at high temperature. This did not affect the numbers of spawning individuals. There was a trend towards lower egg survival to the eyed stage in the 12° C group compared to the 4 and 8° C groups, although the effect was not statistically significant. The results indicate that both the timing of final maturation and investment in ovarian growth in common wolffish are affected by temperature experienced during vitellogenesis.     

Phenological change in a spring ephemeral: implications for pollination and plant reproduction

Climate change has had numerous ecological effects, including species range shifts and altered phenology. Altering flowering phenology often affects plant reproduction, but the mechanisms behind these changes are not well‐understood. To investigate why altering flowering phenology affects plant reproduction, we manipulated flowering phenology of the spring herb Claytonia lanceolata (Portulacaceae) using two methods: in 2011–2013 by altering snow pack (snow‐removal vs. control treatments), and in 2013 by inducing flowering in a greenhouse before placing plants in experimental outdoor arrays (early, control, and late treatments). We measured flowering phenology, pollinator visitation, plant reproduction (fruit and seed set), and pollen limitation. Flowering occurred approx. 10 days earlier in snow‐removal than control plots during all years of snow manipulation. Pollinator visitation patterns and strength of pollen limitation varied with snow treatments, and among years. Plants in the snow removal treatment were more likely to experience frost damage, and frost‐damaged plants suffered low reproduction despite lack of pollen limitation. Plants in the snow removal treatment that escaped frost damage had higher pollinator visitation rates and reproduction than controls. The results of the array experiment supported the results of the snow manipulations. Plants in the early and late treatments suffered very low reproduction due either to severe frost damage (early treatment) or low pollinator visitation (late treatment) relative to control plants. Thus, plants face tradeoffs with advanced flowering time. While early‐flowering plants can reap the benefits of enhanced pollination services, they do so at the cost of increased susceptibility to frost damage that can overwhelm any benefit of flowering early. In contrast, delayed flowering results in dramatic reductions in plant reproduction through reduced pollination. Our results suggest that climate change may constrain the success of early‐flowering plants not through plant‐pollinator mismatch but through the direct impacts of extreme environmental conditions.     

Effect of acclimation temperature on the upper thermal tolerance of Colorado River cutthroat trout Oncorhynchus clarkii pleuriticus: thermal limits of a North American salmonid

In an effort to explore the thermal limitations of Colorado River cutthroat trout Oncorhynchus clarkii pleuriticus, the critical thermal maxima (T_cmax) of 1+ year Lake Nanita strain O. c. pleuriticus were evaluated when acclimated to 10, 15 and 20° C. The mean ±s.d. T_cmax for O. c. pleuriticus acclimated to 10° C was 24·6 ± 2·0°C (n = 30), for 15° C‐acclimated fish was 26·9 ± 1·5° C (n = 23) and for 20° C‐acclimated fish was 29·4 ± 1·1° C (n = 28); these results showed a marked thermal acclimation effect (Q₁₀ = 1·20). Interestingly, there was a size effect within treatments, wherein the T_cmax of larger fish was significantly lower than that of smaller fish acclimated to the same temperature. The critical thermal tolerances of age 0 year O. c. pleuriticus were also evaluated from three separate populations: Lake Nanita, Trapper Creek and Carr Creek reared under ‘common‐garden’ conditions prior to thermal acclimation. The Trapper Creek population had significantly warmer T_cmax than the Lake Nanita population, but that of the Carr Creek fish had T_cmax similar to both Trapper Creek and Lake Nanita fish. A comparison of these O. c. pleuriticus T_cmax results with those of other stream‐dwelling salmonids suggested that O. c. pleuriticus are less resistant to rapid thermal fluctuations when acclimated to cold temperatures, but can tolerate similar temperatures when acclimated to warmer temperatures.     

Temperature has a causal effect on avian timing of reproduction

Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.     

Effects of hypoxia on the thermal physiology of a high-elevation lizard: implications for upslope-shifting species

Montane reptiles are predicted to move to higher elevations in response to climate warming. However, whether upwards-shifting reptiles will be physiologically constrained by hypoxia at higher elevations remains unknown. We investigated the effects of hypoxic conditions on preferred body temperatures (T_pref) and thermal tolerance capacity of a montane lizard (Phrynocephalus vlangalii) from two populations on the Qinghai–Tibet Plateau. Lizards from 2600 m a.s.l. were exposed to O₂ levels mimicking those at 2600 m (control) and 3600 m (hypoxia treatment). Lizards from 3600 m a.s.l. were exposed to O₂ levels mimicking those at 3600 m (control) and 4600 m (hypoxia treatment). The T_pref did not differ between the control and hypoxia treatments in lizards from 2600 m. However, lizards from 3600 m selected lower body temperatures when exposed to the hypoxia treatment mimicking the O₂ level at 4600 m. Additionally, the hypoxia treatment induced lower critical thermal minimum (CT_min) in lizards from both populations, but did not affect the critical thermal maximum (CT_max) in either population. Our results imply that upwards-shifting reptiles may be constrained by hypoxia if a decrease in T_pref reduces thermally dependent fitness traits, despite no observed effect on their heat tolerance.     

The endocrine control of reproduction in Nereidae: a new multi-hormonal model with implications for their functional role in a changing environment

Nereidae are vital to the functioning of estuarine ecosystems and are major components in the diets of over-wintering birds and commercial fish. They use environmental cues to synchronize reproduction. Photoperiod is the proximate cue, initiating vitellogenesis in a temperature-compensated process. The prevailing paradigm in Nereidae is of a single ‘juvenile’ hormone controlling growth and reproduction. However, a new multi-hormone model is presented here that integrates the environmental and endocrine control of reproduction. This is supported by evidence from in vitro bioassays. The juvenile hormone is shown to be heat stable and cross reactive between species. In addition, a second neuro-hormone, identified here as a gonadotrophic hormone, is shown to be present in mature females and is found to promote oocyte growth. Furthermore, dopamine and melatonin appear to switch off the juvenile hormone while serotonin and oxytocin promote oocyte growth. Global warming is likely to uncouple the phase relationship between temperature and photoperiod, with significant consequences for Nereidae that use photoperiod to cue reproduction during the winter in northern latitudes. Genotypic adaptation of the photoperiodic response may be possible, but significant impacts on fecundity, spawning success and recruitment are likely in response to short-term extreme events. Endocrine-disrupting chemicals may also impact on putative steroid hormone pathways in Nereidae with similar consequences. These impacts may have significant implications for the functional role of Nereidae and highlight the importance of comparative endocrinology studies in these and other invertebrates.     

Temperature effect on oxidative stress and egg quality-related genes on post-ovulatory eggs and ovary of red cusk-eel (Genypterus chilensis)

Red cusk-eel (Genypterus chilensis) is a native species with potential for Chilean aquaculture diversification. However, no information exists on the effects of temperature on oxidative stress and eggs quality markers in post-ovulatory eggs and ovary of this species. We determine that high and low temperature generate oxidative damage on post-ovulatory eggs, with no effect on ovary. Temperature induces thermal stress markers expression on post-ovulatory eggs, and modulates antioxidant and eggs quality markers on post-ovulatory eggs and ovary, information to consider for quality evaluation in the red cusk-eel management.     

The effects of inbreeding and heat stress on male sterility in Drosophila melanogaster

Understanding the consequences of inbreeding in combination with stress is important for the persistence of small endangered populations in a changing environment. Inbreeding and stress can influence the population at all stages of the life cycle, and in the last two decades a number of studies have demonstrated inbreeding depression for most life‐cycle components, both in laboratory populations and in the wild. Although male fertility is known to be sensitive to temperature extremes, few studies have focused on this life‐cycle component. We studied the effects of inbreeding on male sterility in benign and stressful environments using Drosophila melanogaster as a model organism. Male sterility was compared in 21 inbred lines and five non‐inbred control lines at 25.0 and 29.0 °C. The effect of inbreeding on sterility was significant only at 29.0 °C. This stress‐induced increase in sterility indicates an interaction between the effects of inbreeding and high‐temperature stress on male sterility. In addition, the stress‐induced temporary and permanent sterility showed significant positive correlation, as did stress‐induced sterility and the decrease in egg‐to‐adult viability. This suggests that the observed stress‐induced decline in fitness could result from conditionally expressed, recessive deleterious alleles affecting both sterility and viability simultaneously. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 432–442.     

Detection of salmonid alphavirus RNA in wild marine fish: implications for the origins of salmon pancreas disease in aquaculture

Salmonid alphaviruses (SAVs), which include the aetiological agents of salmon pancreas disease (SPD) in farmed Atlantic salmon Salmo salar L. and sleeping disease (SD) in rainbow trout Oncorhynchus mykiss (Walbaum), are significant viral pathogens of European salmonid aquaculture. SAV is horizontally transmitted and the virus can survive for extended periods in seawater. A lack of convincing evidence for vertical transmission coupled to the fact that the SPD virus (SPDV) occurs in historically infected sites irrespective of fallow period duration suggests that a substantial reservoir of infection exists in the marine environment. We used a highly sensitive real-time PCR (qPCR) assay targeting a region of the SAV nsP1 gene to screen wild marine fish species for the presence of SAV in an attempt to identify such a potential reservoir. Screened fish species were caught in the vicinity of aquaculture activity in an area with a previous history of SAV infection (Shetland Isles, Scotland). SAV RNA was detected in internal organs (kidney and heart) from the flatfish species common dab Limanda limanda, long rough dab Hippoglossoides platessoides, and plaice Pleuronectes platessa. Based on these findings, sampling was extended to an area remote from aquaculture activity (Stonehaven Bay, NE coast of Scotland) from where heart tissues obtained from common dab also tested positive. While no virus could be cultivated from these samples, qPCR detections were shown to be SAV-specific by sequencing of an alternative gene region (E2) to that targeted by the qPCR assay. Analysis of these nucleotide sequences revealed minor differences to those previously obtained from farmed salmon, and subsequent phylogenetic analysis of an E2 dataset demonstrated a subtype V-like sequence.     

The context dependence of assortative mating: a demonstration with conspecific salmonid populations

Assortative mating is thought to play a key role in reproductive isolation. However, most experimental studies of assortative mating do not take place in multiple natural environments, and hence, they ignore its potential context dependence. We implemented an experiment in which two populations of brown trout (Salmo trutta) with different natural flow regimes were placed into semi‐natural stream channels under two different artificial flow regimes. Natural reproduction was allowed, and reproductive isolation was measured by means of parentage assignment to compare within‐population vs. between‐population male–female mating and relative offspring production. For both metrics, reproductive isolation was highly context dependent: no isolation was evident under one flow regime, but strong isolation was evident under the other flow regime. These patterns were fully driven by variance in the mating success of males from one of the two populations. Our results highlight how reproductive isolation through assortative mating can be strongly context dependent, which could have dramatic consequences for patterns of gene flow and speciation under environmental change.     

Balance between climate change mitigation benefits and land use impacts of bioenergy: conservation implications for European birds

Both climate change and habitat modification exert serious pressure on biodiversity. Although climate change mitigation has been identified as an important strategy for biodiversity conservation, bioenergy remains a controversial mitigation action due to its potential negative ecological and socio-economic impacts which arise through habitat modification by land use change. While the debate continues, the separate or simultaneous impacts of both climate change and bioenergy on biodiversity have not yet been compared. We assess projected range shifts of 156 European bird species by 2050 under two alternative climate change trajectories: a baseline scenario, where the global mean temperature increases by 4 °C by the end of the century, and a 2 degrees scenario, where global concerted effort limits the temperature increase to below 2 °C. For the latter scenario, we also quantify the pressure exerted by increased cultivation of energy biomass as modelled by IMAGE2.4, an integrated land use model. The global bioenergy use in this scenario is in the lower end of the range of previously estimated sustainable potential. Under the assumptions of these scenarios, we find that the magnitude of range shifts due to climate change is far greater than the impact of land conversion to woody bioenergy plantations within the European Union, and that mitigation of climate change reduces the exposure experienced by species. However, we identified potential for local conservation conflict between priority areas for conservation and bioenergy production. These conflicts must be addressed by strict bioenergy sustainability criteria that acknowledge biodiversity conservation needs beyond existing protected areas and apply also to biomass imported from outside the European Union.