Boldness and physiological variation in round goby populations along their Baltic Sea invasion front.

The round goby (Neogobius melanostomus) is a fish native to the Ponto-Caspian region that is highly invasive through freshwater and brackish habitats in northern Europe and North America. Individual behavioural variation appears to be an important factor in their spread, for example a round goby's personality traits can influence their dispersal tendency, which may also produce variation in the behavioral composition of populations at different points along their invasion fronts. To further analyze the drivers of behavioral variation within invasive round goby populations, we focused on two populations along the Baltic Sea invasion front with closely comparable physical and community characteristics. Specifically, this study measured personality within a novel environment and predator response context (i.e., boldness), and directly analyzed links between individuals' personality traits and their physiological characteristics and stress responses (i.e., blood cortisol and lactate, brain neurotransmitters). In contrast to previous findings, the more recently established population had similar activity levels but were less bold in response to a predator cue than the older population, which suggests that behavioral compositions within our study populations may be more driven by local environmental conditions rather than being a result of personality-biased dispersal. Furthermore, we found that both populations showed similar physiological stress responses, and there also appeared to be no detectable relationship between physiological parameters and behavioral responses to predator cues. Instead, body size and body condition were important factors influencing individual behavioral responses. Overall, our results reinforce the importance of boldness traits as a form of phenotypic variation in round goby populations in the Baltic Sea. We also highlight the importance of these traits for future studies specifically testing for effects of invasion processes on phenotypic variation in the species. Nonetheless, our results also highlight that the physiological mechanisms underpinning behavioural variation in these populations remain unclear.

New insights into the recent collapse of Eastern Baltic cod from historical data on stock health.

The Eastern Baltic cod (Gadus morhua) stock is currently in a very poor state, with low biomass and adverse trends in several life history and demographic parameters. This raises concern over whether and to what level recovery is possible. Here, we look for new insights from a historical perspective, extending the time series of various stock health indicators back to the 1940s, i.e. to the beginning of intensive exploitation of the Eastern Baltic cod. The historical data confirm that the stock deterioration in recent years is unprecedented, as all indicators are presently in their worst states on record. Cod body condition and energy reserves were equally low in the 1940s-1950s, accompanied by high parasitic liver worm infection, comparable to that measured in recent years. However, other stock parameters (size structure, size at maturity, stock distribution) are currently in their worst states over the past 80 years. In contrast, the state of cod in the 1970s to early 1990s that is often perceived as a desirable target, was exceptional, with the most favorable indicator levels in the time series. Long-term observation data reveal concurrent or asynchronous trends in different indicators of stock health and to what extent these have coincided with changes in possible external drivers. In this way, the extended time series contribute to ongoing research on understanding the collapse of the cod and its recovery potential.

Bioenergetics modelling of growth processes in parasitized Eastern Baltic cod (Gadus morhua L.).

Changes in physiological processes can reveal how individuals respond to environmental stressors. It can be difficult to link physiological responses to changes in vital rates such as growth, reproduction and survival. Here, bioenergetics modelling can aid in understanding non-intuitive outcomes from stressor combinations. Building on an established bioenergetics model, we examine the potential effects of parasite infection on growth rate and body condition. Parasites represent an overlooked biotic factor, despite their known effects on the physiology of the host organism. As a case study, we use the host-parasite system of Eastern Baltic cod (Gadus morhua) infected with the parasitic nematode Contraceacum osculatum. Eastern Baltic cod have during the past decade experienced increasing infection loads with C. osculatum that have been shown to lead to physiological changes. We hypothesized that infection with parasites affects cod growth negatively as previous studies reveal that the infections lead to reduced energy turnover, severe liver disease and reduced nutritional condition. To test this, we implemented new variables into the bioenergetics model representing the physiological changes in infected fish and parameterized these based on previous experimental data. We found that growth rate and body condition decreased with increased infection load. Highly infected cod reach a point of no return where their energy intake cannot maintain a surplus energy balance, which may eventually lead to induced mortality. In conclusion, parasite infections cannot be ignored when assessing drivers of fish stock dynamics.

Comparative histopathology of livers from Baltic cod infected with the parasitic nematode Contracaecum osculatum.

Infection levels with the parasitic nematode Contracaecum osculatum in Eastern Baltic cod have increased in the last decades. Eastern Baltic cod is transport host for this parasite that has a high affinity for the liver of the fish. The liver is a highly vital organ and damage to the liver tissue can result in reduced functionality of the organ. Previous studies have revealed that cod with high infections loads reveal impaired physiological performance, reduced nutritional condition and show signs of having a liver disease. Yet, little is known about the pathological changes and inflammatory reactions of the cod liver related to the infections. In this study, we performed histological examinations on 30 Baltic cod livers caught in the eastern part of the Baltic Sea (length; 38 ± 0.9 cm, weight; 454 ± 34.8 gram) and three Sound cod livers (length; 63 ± 2.9 cm, weight; 3396 ± 300.2 gram) to categorize the degree of inflammation and its relation to pathological changes in infected cod livers. We further investigated how C. osculatum infection levels varied with intensity of inflammation and co-infections. We found that high infection loads with C. osculatum caused severe inflammation in the liver tissue of cod and reduced fat content of the hepatocytes. Conspicuous amounts of glycogen were found in the muscle and intestinal epithelial cells of the nematodes and parasitic co-infections occurred more frequently in the most heavily infected livers.

Aerobic metabolic scope mapping of an invasive fish species with global warming.

Climate change will exacerbate the negative effects associated with the introduction of non-indigenous species in marine ecosystems. Predicting the spread of invasive species in relation to environmental warming is therefore a fundamental task in ecology and conservation. The Baltic Sea is currently threatened by several local stressors and the highest increase in sea surface temperature of the world's large marine ecosystems. These new thermal conditions can further favour the spreading of the invasive round goby (Neogobius melanostomus), a fish of Ponto-Caspian origin, currently well established in the southern and central parts of the Baltic Sea. This study aims to assess the thermal habitat suitability of the round goby in the Baltic Sea considering the past and future conditions. The study combines sightings records with known physiological models of aerobic performance and sea surface temperatures. Physiological models read these temperatures, at sighting times and locations, to determine their effects on the aerobic metabolic scope (AMS) of the fish, a measure of its energetic potential in relation to environmental conditions. The geographical mapping of the AMS was used to describe the changes in habitat suitability during the past 3 decades and for climatic predictions (until 2100) showing that the favourable thermal habitat in the Baltic Sea has increased during the past 32 years and will continue to do so in all the applied climate model predictions. Particularly, the predicted new thermal conditions do not cause any reduction in the AMS of round goby populations, while the wintertime cold ranges are likely expected to preserve substantial areas from invasion. The results of this research can guide future monitoring programs increasing the chance to detect this invader in novel areas.

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe.

For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salinity from a freshwater and a brackish population within their ancestral Ponto-Caspian region of the round goby, Neogobius melanostomus. These two ancestral populations were then compared to nine additional invaded sites across northern Europe, both in terms of their sperm traits and by using genomic SNP markers. Our results show clear patterns of ancestral adaptations to freshwater and brackish salinities in their sperm performance. Population genomic analyses show that the ancestral ecotypes have generally established themselves in environments that fit their sperm adaptations. Sites close to ports with intense shipping show that both outbreeding and admixture can affect the sperm performance of a population in a given salinity. Rapid adaptation to local conditions is also supported at some sites. Historical and contemporary evolution in the traits of the round goby sperm cells is tightly linked to the population and seascape genomics as well as biogeographic processes in these invasive fishes. Since the risk of a population establishing in an area is related to the genotype by environment match, port connectivity and the ancestry of the round goby population can likely be useful for predicting the species spread.

Personality-dependent inter- and intraspecific foraging competition in the invasive round goby, Neogobius melanostomus.

This study examines the impact of boldness on foraging competition of the highly invasive round goby Neogobius melanostomus Pallas 1815. Individual risk tolerance, or boldness, was measured as the time to resume movement after a simulated predation strike. Fish that resumed movement faster were categorized as "bold," fish that took more time to resume movement were categorized as "shy" and those that fell in between these two categories were determined to have "intermediate" boldness. Competitive impacts of boldness in N. melanostomus were determined in a laboratory foraging experiment in which interspecific (juvenile Atlantic cod Gadus morhua Linnaeus 1758) and intraspecific (intermediate N. melanostomus) individuals were exposed to either bold or shy N. melanostomus competitors. G. morhua consumed fewer prey when competing with bold N. melanostomus than when competing with shy N. melanostomus, whereas intermediately bold N. melanostomus foraging was not affected by competitor boldness. Bold and shy N. melanostomus consumed similar amounts of prey, and the number of interactions between paired fish did not vary depending on the personality of N. melanostomus individuals. Therefore, intraspecific foraging competition was not found to be personality dependent. This study provides evidence that individual differences in boldness can mediate competitive interactions in N. melanostomus; nonetheless, results also show that competition is also governed by other mechanisms that require further study.

Effects of temperature on physiological performance and behavioral thermoregulation in an invasive fish, the round goby.

Invasive species exert negative impacts on biodiversity and ecosystems on a global scale, which may be enhanced in the future by climate change. Knowledge of how invasive species respond physiologically and behaviorally to novel and changing environments can improve our understanding of which traits enable the ecological success of these species, and potentially facilitate mitigation efforts. We examined the effects of acclimation to temperatures ranging from 5 to 28°C on aerobic metabolic rates, upper temperature tolerance (critical thermal maximum, CTmax), as well as temperature preference (Tpref) and avoidance (Tavoid) of the round goby (Neogobius melanostomus), one of the most impactful invasive species in the world. We show that round goby maintained a high aerobic scope from 15 to 28°C; that is, the capacity to increase its aerobic metabolic rate above that of its maintenance metabolism remained high across a broad thermal range. Although CTmax increased relatively little with acclimation temperature compared with other species, Tpref and Tavoid were not affected by acclimation temperature at all, meaning that round goby maintained a large thermal safety margin (CTmax-Tavoid) across acclimation temperatures, indicating a high level of thermal resilience in this species. The unperturbed physiological performance and high thermal resilience were probably facilitated by high levels of phenotypic buffering, which can make species readily adaptable and ecologically competitive in novel and changing environments. We suggest that these physiological and behavioral traits could be common for invasive species, which would only increase their success under continued climate change.

Physiological condition of Eastern Baltic cod, Gadus morhua, infected with the parasitic nematode Contracaecum osculatum.

Establishing relationships between parasite infection and physiological condition of the host can be difficult and therefore are often neglected when describing factors causing population declines. Using the parasite-host system between the parasitic nematode Contracaecum osculatum and the Eastern Baltic cod Gadus morhua, we here shed new light on how parasite load may relate to the physiological condition of a transport host. The Eastern Baltic cod is in distress, with declining nutritional conditions, disappearance of the larger fish, high natural mortality and no signs of recovery of the population. During the latest decade, high infection levels with C. osculatum have been observed in fish in the central and southern parts of the Baltic Sea. We investigated the aerobic performance, nutritional condition, organ masses, and plasma and proximate body composition of wild naturally infected G. morhua in relation to infection density with C. osculatum. Fish with high infection densities of C. osculatum had (i) decreased nutritional condition, (ii) depressed energy turnover as evidenced by reduced standard metabolic rate, (iii) reduction in the digestive organ masses, and alongside (iv) changes in the plasma, body and liver composition, and fish energy source. The significantly reduced albumin to globulin ratio in highly infected G. morhua suggests that the fish suffer from a chronic liver disease. Furthermore, fish with high infection loads had the lowest Fulton's condition factor. Yet, it remains unknown whether our results steam from a direct effect of C. osculatum, or because G. morhua in an already compromised nutritional state are more susceptible towards the parasite. Nevertheless, impairment of the physiological condition can lead to reduced swimming performance, compromising foraging success while augmenting the risk of predation, potentially leading to an increase in the natural mortality of the host. We hence argue that fish-parasite interactions must not be neglected when implementing and refining strategies to rebuild deteriorating populations.

Personality- and size-related metabolic performance in invasive round goby (Neogobius melanostomus).

Differences between individuals in behavioral type (i.e. animal personality) are ecologically and evolutionarily important because they can have significant effects on fitness components such as growth and predation risk. In the present study we are used the invasive round goby (Neogobius melanostomus) from an established population in controlled experiments to examine the relationships among personality, metabolic performance, and growth rate (inferred as size-at-age). Boldness was measured as the time to return to normal behavior after a simulated predator attack, where fish with shorter freezing times were categorized as "bold" and fish with longer times were categorized as "shy." We show that bold fish have significantly higher standard metabolic rate (SMR) than their shy conspecifics, whereas there was no difference between personality types in their maximum metabolic rate (MMR) or aerobic scope (AS). Bold fish furthermore had a smaller size-at-age as compared to shy fish. Together this provides evidence of a metabolic underpinning of personality where the high-SMR bold fish require more resources to sustain basic life functions than their low-SMR shy conspecifics, indicating that bold round goby from established populations with high densities (and high competition for food) pay a price of reduced growth rate.

Evaluating dispersal potential of an invasive fish by the use of aerobic scope and osmoregulation capacity.

Non-indigenous species (NIS) can impact marine biodiversity and ecosystem structure and function. Once introduced into a new region, secondary dispersal is limited by the physiology of the organism in relation to the ambient environment and by complex interactions between a suite of ecological factors such as presence of predators, competitors, and parasites. Early prediction of dispersal potential and future 'area of impact' is challenging, but also a great asset in taking appropriate management actions. Aerobic scope (AS) in fish has been linked to various fitness-related parameters, and may be valuable in determining dispersal potential of aquatic invasive species in novel environments. Round goby, Neogobius melanostomus, one of the most wide-ranging invasive fish species in Europe and North America, currently thrives in brackish and fresh water, but its ability to survive in high salinity waters is unknown to date. We show that AS in round goby is reduced by 30% and blood plasma osmolality increased (indicating reduced capacity for osmoregulation) at salinities approaching oceanic conditions, following slow ramping (5 PSU per week) and subsequent long-term acclimation to salinities ranging between 0 and 30 PSU (8 days at final treatment salinities before blood plasma osmolality measurements, 12-20 additional days before respirometry). Survival was also reduced at the highest salinities yet a significant proportion (61%) of the fish survived at 30 PSU. Reduced physiological performance at the highest salinities may affect growth and competitive ability under oceanic conditions, but to what extent reduced AS and osmoregulatory capacity will slow the current 30 km year-1 rate of advance of the species through the steep salinity gradient from the brackish Baltic Sea and into the oceanic North Sea remains speculative. An unintended natural experiment is in progress to test whether the rate of advance slows down. At the current rate of advance the species will reach the oceanic North Sea by 2018/2019, therefore time for taking preventative action is short.

Consequences of eye fluke infection on anti-predator behaviours in invasive round gobies in Kalmar Sound.

Larvae of the eye fluke, Diplostomum, emerge from snails and infect fish by penetrating skin or gills, then move to the lens where they may impair the vision of the fish. For the fluke to reproduce, a bird must eat the infected fish, and it has been suggested that they therefore actively manipulate the fish's behaviour to increase the risk of predation. We found that round gobies Neogobius melanostomus, a species that was recently introduced to the Kalmar Sound of the Baltic Sea, had an eye fluke prevalence of 90-100%. We investigated how the infection related to behavioural variation in round gobies. Our results showed that the more intense the parasite-induced cataract, the weaker the host's response was to simulated avian attack. The eye flukes did not impair other potentially important anti-predator behaviours, such as shelter use, boldness and the preference for shade. Our results are in accordance with the suggestion that parasites induce changes in host behaviour that will facilitate transfer to their final host.

The effect of temperature and body size on metabolic scope of activity in juvenile Atlantic cod Gadus morhua L.

Changes in ambient temperature affect the physiology and metabolism and thus the distribution of fish. In this study we used intermittent flow respirometry to determine the effect of temperature (2, 5, 10, 15 and 20°C) and wet body mass (BM) (~30-460g) on standard metabolic rate (SMR, mgO2h(-1)), maximum metabolic rate (MMR, mgO2h(-1)) and metabolic scope (MS, mgO2h(-1)) of juvenile Atlantic cod. SMR increased with BM irrespectively of temperature, resulting in an average scaling exponent of 0.87 (0.82-0.92). Q10 values were 1.8-2.1 at temperatures between 5 and 15°C but higher (2.6-4.3) between 2 and 5°C and lower (1.6-1.4) between 15 and 20°C in 200 and 450g cod. MMR increased with temperature in the smallest cod (50g) but in the larger cod MMR plateaued between 10, 15 and 20°C. This resulted in a negative correlation between the optimal temperature for MS (Topt) and BM, Topt being respectively 14.5, 11.8 and 10.9°C in a 50, 200 and 450g cod. Irrespective of BM cold water temperatures resulted in a reduction (30-35%) of MS whereas the reduction of MS at warm temperatures was only evident for larger fish (200 and 450g), caused by plateauing of MMR at 10°C and above. Warm temperatures thus seem favourable for smaller (50g) juvenile cod, but not for larger conspecifics (200 and 450g).

Haemoglobin genotypes in cod (Gadus morhua L): their geographic distribution and physiological significance.

Haemoglobin polymorphism in cod (Gadus morhua L) has been investigated throughout the last 50years. Field studies have shed light on the geographic distribution of the two common alleles (HbI(1) and HbI(2)), and laboratory studies have shown effects of genotype on physiological traits such as growth, reproduction and hypoxia tolerance. The geographic distribution of alleles shows a correlation with temperature, with increasing frequency of HbI(1) in warmer areas. This is likely due to temperature-related differences in oxygen affinity of the three genotypes. We provide a general ecological introduction to cod haemoglobin polymorphism and a detailed discussion of physiological studies, particularly laboratory growth studies. Although differences in oxygen uptake are almost certainly a contributory mechanism to observed differences in traits such as growth rate, many other environmental, behavioural and social factors may also contribute, making it difficult to quantify the effect of HbI either experimentally or in the field.

Effects of hypoxic exposure during feeding on SDA and postprandial cardiovascular physiology in the Atlantic cod, Gadus morhua.

Some Atlantic cod in the Bornholm Basin undertake vertical foraging migrations into severely hypoxic bottom water. Hypoxic conditions can reduce the postprandial increase in gastrointestinal blood flow (GBF). This could subsequently postpone or reduce the postprandial increase in oxygen consumption (MO(2)), i.e. the SDA, leading to a disturbed digestion. Additionally, a restricted oxygen uptake could result in an oxygen debt that needs to be compensated for upon return to normoxic waters and this may also affect the ability to process the food. Long-term cardio-respiratory measurements were made on fed G. morhua in order to understand how the cardio-respiratory system of feeding fish respond to a period of hypoxia and a subsequent return to normoxia. These were exposed to 35% water oxygen saturation for 90 minutes, equivalent to the time and oxygen level cod voluntarily endure when searching for food in the Bornholm Basin. We found that i) gastric and intestinal blood flows, cardiac output and MO(2) increased after feeding, ii) gastric and intestinal blood flows were spared in hypoxia, and iii) there were no indications of an oxygen debt at the end of the hypoxic period. The magnitude and time course of the measured variables are similar to values obtained from fish not exposed to the hypoxic period. In conclusion, when cod in the field search for and ingest prey under moderate hypoxic conditions they appear to stay within safe limits of oxygen availability as we saw no indications of an oxygen debt, or negative influence on digestive capacity, when simulating field observations.

Thermodynamics of oxygenation-linked proton and lactate binding govern the temperature sensitivity of O2 binding in crustacean (Carcinus maenas) hemocyanin.

With the aim of understanding the molecular underpinnings of the enormous variation in the temperature sensitivity of hemocyanin-O2 affinity encountered in crustaceans, we measured O2 binding to Carcinus maenas hemocyanin at two temperatures, varying pH values and in the absence and presence of lactate ions in order to assess the contributions of oxygenation-linked binding of protons (the Bohr effect) and lactate ions to the overall enthalpies of oxygenation (DeltaH'). The hemocyanin binds maximally 0.35 lactate ions per functional subunit. Lactate (which accumulates under hypoxic conditions) increases O2 affinity by preferentially raising the association equilibrium constant of the hemocyanin in the low-affinity Tense state (KT), without significantly affecting that of the high-affinity Relaxed state (KR). In the absence of lactate, the variation in the temperature sensitivity observed with decreasing pH tallies neatly with changes in the nature and magnitude of the Bohr effect. Accordingly, the normal, absent and reverse Bohr effects observed under alkaline, neutral and acid conditions, respectively, reflect endothermic proton dissociation, absence of proton binding and exothermic proton association, respectively, upon oxygen binding. Oxygenation-linked lactate binding is exothermic, highly pH dependent and peaks near pH 7.6, where it contributes approximately -30 kJ mol(-1) to the overall heat of oxygenation. This predictably increases the temperature sensitivity of O2 affinity, potentially hampering O2 loading in warm, hypoxic habitats. The data demonstrate governing roles for lactate and proton ions in determining the temperature sensitivity of hemocyanin-O2 affinity in crustaceans.

Oxygen dynamics around buried lesser sandeels Ammodytes tobianus (Linnaeus 1785): mode of ventilation and oxygen requirements.

The oxygen environment around buried sandeels (Ammodytes tobianus) was monitored by planar optodes. The oxygen penetration depth at the sediment interface was only a few mm. Thus fish, typically buried at 1-4 cm depth, were generally in anoxic sediment. However, they induced an advective transport through the permeable interstice and formed an inverted cone of porewater with 93% air saturation in front of the mouth. From dye experiments the mean ventilatory flow rate was estimated at 0.26+/-0.02 ml min(-1) (86.9+/-7.3 ml min(-1) kg(-1)) (N=3). Expelled water from the gills induced a 1 cm circular plume with <15% air saturation around the gills. During this quasi-steady ventilation mode, fish extracted 86.2+/-4.8% (N=7) of the oxygen from the inspired water. However, 13% of the investigated fish (2 of 15) occasionally wriggled their bodies and thereby transported almost fully air-saturated water down along the body, referred to as ;plume ventilation'. Yet, within approximately 30 min the oxic plume was replenished by oxygen-depleted water from the gills. The potential for cutaneous respiration by the buried fish was thus of no quantitative importance. Calculations derived by three independent methods (each with N=3) revealed that the oxygen uptake of sandeel buried for 6-7 h was 40-50% of previous estimates on resting respirometry of non-buried fish, indicating lower O(2) requirements during burial on a diurnal timescale. Buried fish exposed to decreasing oxygen tensions gradually approached the sediment surface, but remained in the sediment until the inspired water reached 5-10% air saturation.

The archaeogastropod mollusc Haliotis iris: tissue and blood metabolites and allosteric regulation of haemocyanin function.

We investigated divalent cation and anaerobic end-product concentrations and the interactive effects of these substances and pH on haemocyanin oxygen-binding (Hc-O(2)) in the New Zealand abalone Haliotis iris. During 24 h of environmental hypoxia (emersion), D-lactate and tauropine accumulated in the foot and shell adductor muscles and in the haemolymph of the aorta, the pedal sinus and adductor muscle lacunae, whereas L-lactate was not detected. Intramuscular and haemolymph D-lactate concentrations were similar, but tauropine accumulated to much higher levels in muscle tissues. Repeated disturbance and short-term exposure to air over 3 h induced no accumulation of D- or L-lactate and no change in [Ca(2+)], [Mg(2+)], pH and O(2)-binding properties of the native haemolymph. The haemolymph showed a low Hc-O(2) affinity, a large reverse Bohr effect and marked cooperativity. Dialysis increased Hc-O(2) affinity, obliterated cooperativity and decreased the pH-sensitivity of O(2) binding. Replacing Mg(2+) and Ca(2+) restored the native O(2)-binding properties and the reverse Bohr shift. L- and D-lactate exerted minor modulatory effects on O(2)-affinity. At in vivo concentrations of Mg(2+) and Ca(2+), the cooperativity is dependent largely on Mg(2+), which modulates the O(2) association equilibrium constants of both the high-affinity (K(R)) and the low-affinity (K(T)) states (increasing and decreasing, respectively). This allosteric mechanism contrasts with that encountered in other haemocyanins and haemoglobins. The functional properties of H. iris haemocyanin suggest that high rates of O(2) delivery to the tissues are not a priority but are consistent with the provision of a large O(2) reserve for facultatively anaerobic tissues during internal hypoxia associated with clamping to the substratum.