Peculiarities of functioning of liver mitochondria of river lamprey Lampetra fluviatilis and common frog Rana temporaria at periods of suppression and activation of energy metabolism

The work dealt with study of mitochondria in reversible metabolic suppression of hepatocytes of the river lamprey Lampetra fluviatilis in the course of prespawning starvation and of liver mitochondria of the common frog Rana temporaria during hibernation and activity. In winter the metabolic depression of lamprey hepatocytes, unlike that of frog hepatocytes, has been found to be due to deactivation of complex I of the electron transport mitochondrial chain, a low rate of NAD-dependent substrate oxidation, a low content of adenine nucleotide content, and a high degree of mitochondrial membrane permeability to H+ and other monovalent ions (KCl-, K+). The mitochondrial membrane permeability decreases in the presence of ethyleneglycoldiamineethyltetraacetic acid (EGTA), cyclosporine A (CsA), adenosine-5'-diphosphate (ADP), and Mg+. These facts indicate the presence in these mitochondria of the Ca2+ -dependent unspecific pore in the low-conductance state. Histological studies showed the lamprey and the frog to have principal differences in use of energy substrates at the period of metabolic depression. Lampreys utilize predominantly lipids, whereas frogs--glycogen. The clearly pronounces activation of lipid consumption is observed at the spring period before spawning and death of lamprey. Possible causes of metabolic depression are discussed as well as similarity and difference in behavior of mitochondria of cyclostomes and amphibians throughout metabolic depression and activity.     

Peculiarities of functioning of liver mitochondria of the river lamprey <Emphasis Type="Italic">Lampetra fluviatilis</Emphasis> and the common frog <Emphasis Type="Italic">Rana temporaria</Emphasis> at periods of suppression and activation of energy metabolism

The work dealt with study of mitochondria in reversible metabolic suppression of heap-tocytes of the river lamprey Lampetra fluviatilis in the course of prespawning starvation and of liver mitochondria of the common frog Rana temporaria during hibernation and activity. In winter the metabolic depression of lamprey hepatocytes, unlike that of frog hepatocytes, has been found to be due to deactivation of complex I of the electron transport mitochondrial chain, a low rate of NAD-dependent substrate oxidation, a low content of adenine nucleotide content, and a high degree of mitochondrial membrane permeability to H⁺ and other monovalent ions (KCl^–, K⁺). The mitochondrial membrane permeability decreases in the presence of ethyleneglycoldiamineethyltetraacetic acid (EGTA), cyclosporine A (CsA), adenosine-5′-diphosphate (ADP), and Mg²⁺. These facts indicate the presence in these mitochondria of the Ca²⁺-dependent unspecific pore in the low-conductance state. Histological studies showed the lamprey and the frog to have principal differences in use of energy substrates at the period of metabolic depression. Lampreys utilize predominantly lipids, whereas frogs—glycogen. The clearly pronounced activation of lipid consumption is observed at the spring period before spawning and death of lamprey. Possible causes of metabolic depression are discussed as well as similarity and difference in behavior of mitochondria of cyclostomes and amphibians throughout depression and activity.     

Reversible metabolic depression in hepatocytes of lamprey (Lampetra fluviatilis) during pre-spawning: regulation by substrate availability

The regulation of oxidative metabolism in hepatocytes of lampreys (Lampetra fluviatilis) during the freshwater pre-spawning period of their life cycle was studied. The energy metabolism in these cells is characterized by a simplified scheme, where glycolytic ATP production is insignificant and fatty acids are the major respiratory substrates. Seasonal changes in aerobic cell metabolism include a considerable reversible depression of metabolic rate in lamprey hepatocytes during the winter months of the pre-spawning period. The depression is characterized by a more than twofold decrease in hepatocyte endogenous respiration rate, a reduction of oxidative phosphorylation and drop in cellular ATP content. The addition of fatty acids to the hepatocyte incubation medium prevents the decrease in the metabolic rate. In spring, before spawning, a marked activation of energy metabolism in lamprey hepatocytes is found. These observations support the conclusion that the regulation of lamprey hepatocyte energy metabolism is realized through the availability of fatty acids for oxidation.     

Bioenergetic parameters of lamprey and frog liver mitochondria during metabolic depression and activity

The objective of this study is to elucidate the role of mitochondria in reversible metabolic depression of hepatocytes of the Baltic lamprey (Lampetra fluviatilis) taking place in the last year of its life cycle and to compare their main bioenergetic parameters with those of the frog (Rana temporaria) and the white outbred mouse (Mus musculus). Using isolated mitochondria as a model, we have revealed significant seasonal variations in the main bioenergetic parameters of the lamprey liver. These changes indicate that the metabolic depression is mediated by prolonged reversible alterations of mitochondrial functions, which manifest in low activity of the mitochondrial respiratory chain, low oxidative phosphorylation, low content of mitochondrial adenine nucleotides, high level of reduced mitochondrial pyridine nucleotides and leaky mitochondrial membranes observed in winter. The enhanced ion membrane permeability of winter lamprey liver mitochondria is found to be sensitive to EGTA and to cyclosporine A in combination with ADP and Mg²⁺ and is likely mediated opening the mitochondrial permeability transition pore in its low conductance state. The sharp activation of oxidation and phosphorylation in the lamprey liver mitochondria followed by spawning and death of the animal is observed in spring. The possible causes of the phenomenon and the differences obtained between lamprey, frog and mouse are under discussion.     

The exception to the rule: retreating ice front makes Bewick's swans Cygnus columbianus bewickii migrate slower in spring than in autumn

In the vast majority of migratory bird species studied so far, spring migration has been found to proceed faster than autumn migration. In spring, selection pressures for rapid migration are purportedly higher, and migratory conditions such as food supply, daylength, and/or wind support may be better than in autumn. In swans, however, spring migration appears to be slower than autumn migration. Based on a comparison of tundra swan Cygnus columbianus tracking data with long‐term temperature data from wheather stations, it has previously been suggested that this was due to a capital breeding strategy (gathering resources for breeding during spring migration) and/or to ice cover constraining spring but not autumn migration. Here we directly test the hypothesis that Bewick's swans Cygnus columbianus bewickii follow the ice front in spring, but not in autumn, by comparing three years of GPS tracking data from individual swans with concurrent ice cover data at five important migratory stop‐over sites. In general, ice constrained the swans in the middle part of spring migration, but not in the first (no ice cover was present in the first part) nor in the last part. In autumn, the swans migrated far ahead of ice formation, possibly in order to prevent being trapped by an early onset of winter. We conclude that spring migration in swans is slower than autumn migration because spring migration speed is constrained by ice cover. This restriction to spring migration speed may be more common in northerly migrating birds that rely on freshwater resources.     

D-Glucose uptake in fish hepatocytes: mediated by transporter in rainbow trout (Oncorhynchus mykiss), but only by diffusion in prespawning lamprey (Lampetra fluviatilis) and in RTH-149 cell line

The transport of D-glucose into rainbow trout (Oncorhynchus mykiss) and river lamprey (Lampetra fluviatilis) hepatocytes, as well as into rainbow trout hepatoblastoma cell line RTH-149 was studied using tracer methods. The half-time for D-glucose equilibration was 15 s for rainbow trout. The half-times for the non-metabolizable D-glucose analog, 3-O-methyl-D-glucose equilibration were 8 s, 37 s and 38 s for rainbow trout, lamprey and RTH-149 cells, respectively. The 3-O-methyl-D-glucose was taken up by rainbow trout hepatocytes by facilitated diffusion in addition to simple diffusion. The uptake showed saturation kinetics with the K(m) of 37 mM and V(max) of 62 mmol kg(-1) cells min(-1). The uptake was sensitive to phloretin and cytochalasin B, but not affected by ouabain. The 3-O-methyl-D-glucose uptake by lamprey hepatocytes and RTH-149 cells showed no indication of saturation up to 160 mM, and was not affected by phloretin, cytochalasin B or ouabain, which suggests the mode of transport to be by passive diffusion. However, immunocytochemical stainings revealed the existence of mammalian type GLUT1 and GLUT2 transporters in all cells studied. The lack of a functioning carrier-mediated glucose uptake in lamprey hepatocytes might be due to its physiological state (prespawning starvation). The minor 3-O-methyl-D-glucose uptake into RTH-149 cells compared to freshly isolated rainbow trout hepatocytes might reflect low metabolic activity of the cell lines. Under the conditions applied the RTH-149 cell line is no suitable in vitro model for glucose transport in fish cells.     

Using visible implant elastomer to study ammocoete populations with Cormack–Jolly–Seber models

This study examined the efficacy of marking wild populations of lampreys with visible implant elastomer (VIE) for 6–18 months to examine ammocoete movements using Cormack–Jolly–Seber (CJS) open‐population models. These methods were tested on two lamprey populations in different river systems. American brook lamprey Lethenteron appendix at Dyke Creek apparent survival (φ) was high in the summer and winter (c. 0·7), but declined after flow events in the spring and autumn. Sea lamprey Petromyzon marinus at Oquaga Creek φ in the top‐ranked models varied with stream location and time. Estimates of φ were similar to Dyke Creek during the summer (c. 0·7), but declined after flow events and remained low (c. 0·1) in winter. Open‐population models support current understanding of ammocoete movement, i.e. dispersal is driven by high‐flow events at certain times of the year. The present study provides a framework to study ammocoetes with VIE.     

Manipulation of the energetic state of Atlantic salmon Salmo salar juveniles and the effect on migration speed

Atlantic salmon Salmo salar smolts were produced with similar energetic states as wild S. salar and the effect of low energetic state on smolt migration was tested. The total energetic state of the fish (body lipids and proteins) in the spring was correlated with Fulton's condition factor (K). Fish at a low energetic state swam slower but migrated further than fish at a higher energetic state when tested in two experimental streams. During a period of starvation throughout the winter and spring, fish conserved their body‐lipid reserves at 1·5% by using more protein as an energy source and the metabolic shift occurred between 3·5 and 1·5% body lipids. An energetic state of approximately 3·5 kJ g^?1 (K ≈ 0·65) appeared to be the critical limit for survival.     

Mitochondrial and lysosomal pathways of lamprey (Lampetra fluviatilis L.) hepatocyte death

Mechanisms of mitochondrial and lysosomal pathways of natural death of lamprey hepatocytes are described at the spring period of the prespawn migration. The mitochondrial pathway (release of cytochrome c from mitochondria into cytosol and activation of caspases) is realized by the classic scheme of apoptosis. Comparatively recently, the lysosomal pathway of cell death associated with cathepsin B activation has been revealed in cells in pathologies, specifically in obstruction of gallbladder and bile ducts. A peculiarity of lamprey hepatocytes consists in that in the adult animal liver there takes place biliary atresia (the absence of gallbladder and bile ducts. Thereby, the lamprey hepatocytes are an excellent object for study of this new pathway of cell death. We have revealed development of the mitochondrial and the lysosomal pathways of cell death of lamprey hepatocytes.     

Seasonal energy utilization in bamboo by the red panda (Ailurus fulgens)

Seasonal energy intake and digestion of bamboo by red pandas were measured in energy balance trials at the field station at an altitude of 3,100 m in Yele Natural Reserve, Mianning County of Sichuan Province, Peoples Republic of China. Two‐week trials were conducted at monthly intervals by feeding animals with only natural bamboo browse, Bashania spanostachya, from May to November 1995. Results demonstrated that energy intake, digestible energy, and digestibility differed significantly among seasons and diets. Energy digestibilities were high in summer‐autumn, intermediate in spring, and low in winter. These variations correlated positively with the nutrient contents of bamboo. The daily metabolic energy requirement measured varied from 2,603.3 kJ in the spring to 3,139.8 kJ in the summer‐autumn to 2,740.8 kJ in the winter. The results also showed that shoots were more easily digested than leaves and exhibited the highest digestibility. Restricted by the capacity of digestive tracts, red pandas poorly utilized the energy provided by bamboo as indicated by the lower energy digestibility (averaging 26.47% for leaves and 44.08% for shoots among the seasons). To fulfill their daily energy requirements, red pandas ingested a large amount of energy from bamboo leaves, which varied from 10,145.8 kJ in the spring, 12,045.1 kJ in the summer‐autumn, and 12,276.9 kJ in the winter to maximize the rate of energy intake. Zoo Biol 19:27–33, 2000. © 2000 Wiley‐Liss, Inc.     

Migration patterns of Hoopoe Upupa epops and Wryneck Jynx torquilla: an analysis of European ring recoveries

For many bird species, recovery of ringed individuals remains the best source of information about their migrations. In this study, we analyzed the recoveries of ringed European Hoopoe (Upupa epops) and the Eurasian Wryneck (Jynx torquilla) from 1914 to 2005 from all European ringing schemes. The aim was to define general migration directions and to make inferences about the winter quarters, knowing that hardly any recoveries are available from sub-Saharan Africa. For the autumn migration, there is evidence of a migratory divide for the Hoopoe in Central Europe, at approximately 10–12°E. Autumn migration directions of Wrynecks gradually change from SW to SE depending on the longitude (west to east) of the ringing place. In both species, only a few recoveries were available indicating spring migration directions, but they showed similar migration axes as for autumn migration, and hence no evidence for loop-migration. Due to a paucity of recoveries on the African continent, we can make only limited inferences about wintering grounds: extrapolating migration directions are only indicative of the longitude of the wintering area. The directions of autumn migration indicate a typical pattern observed in European long-distance migrants: west-European Hoopoes and Wrynecks are likely to winter in western Africa, while central- and east-European birds probably winter more in the east. Due to the migratory divide, for the Hoopoe, this phenomenon is more pronounced.     

黑线仓鼠体重和能量代谢的季节性变化

为阐明小型哺乳动物体重和能量代谢的季节性变化以及生理调节机制,将黑线仓鼠驯化于自然环境下12个月,测定其体重、能量收支、身体组织器官和血清瘦素水平的季节性变化。黑线仓鼠能量摄入和支出的季节性变化显著,冬季摄入能、基础代谢率(BMR)、非颤抖性产热(NST)显著高于夏季。体重季节性变化不显著,但身体组织器官重量呈现显著的季节性变化,冬季肝脏、心脏、肾脏以及消化道重量显著高于夏季。体脂含量夏季最高,冬季最低,冬季显著低于夏、秋和春季(P <0.01)。血清瘦素水平的季节性变化显著,夏季瘦素水平比秋、冬季分别高88.2% 和52.4% (P <0.05)。结果表明,黑线仓鼠体重维持季节性稳定,与“调定点假说”的预测不同;但脂肪含量和血清瘦素季节性变化显著,符合该假说。夏季血清瘦素升高具有抑制能量摄入的作用,冬季血清瘦素可能是促进代谢产热的重要因子,瘦素对能量代谢和体重的调节作用与气候的季节性变化有关。       

Food constraints explain the restricted distribution of wintering Lesser White‐fronted Geese Anser erythropus in China

More than 90% of the Lesser White‐fronted Geese Anser erythropus in the Eastern Palearctic flyway population winter at East Dongting Lake, China. To explain this restricted distribution and to understand better the winter feeding ecology and habitat requirements of this poorly known species, we assessed their food availability, diet and energy budgets at this site through two winters. Lesser White‐fronted Geese maintained a positive energy budget when feeding on above‐ground green production of Eleocharis and Alopecurus in recessional grasslands in autumn and spring to accumulate fat stores. Such food was severely depleted by late November and showed no growth in mid‐winter. Geese fed on more extensive old‐growth Carex sedge meadows in mid‐winter where they were in energy deficit and depleted endogenous fat stores. Geese failed to accumulate autumn fat stores in one year when high water levels prevented the Geese from using recessional grassland feeding areas. Fat stores remained lower throughout that winter and Geese left for breeding areas later in spring than in the previous year, perhaps reflecting the need to gain threshold fat stores for migration. Sedge meadows are widespread at other Yangtze River floodplain wetlands, but recessional grasslands are rare and perhaps restricted to parts of East Dongting Lake, which would explain the highly localized distribution of Lesser White‐fronted Geese in China and their heavy use of these habitats at this site. Sympathetic management of water tables is essential to maintain the recessional grasslands in the best condition for Geese. Regular depletion of fat stores whilst grazing sedge meadows in mid‐winter also underlines the need to protect the species from unnecessary anthropogenic disturbances that enhance energy expenditure. The specialized diet of the Lesser White‐fronted Goose may explain its highly restricted winter distribution and global rarity.     

To fast or feed: an alternative life history for anadromous brook trout Salvelinus fontinalis overwintering within a harbour

The seasonal feeding pattern of sea‐run brook trout Salvelinus fontinalis was studied from November to May 2010–2012 in Antigonish Harbour, Nova Scotia, Canada (45° 38′ N; 61° 55′ W). Sixty‐three S. fontinalis (mean ± s.d . fork length = 330 ± 70 mm and mass = 536 ± 351 g) captured had fed predominantly on fishes (Fundulidae and Gasterosteidae). Percentage of empty stomachs was highest during autumn (18%) and winter (22%) and lowest in spring (7%). Stomach fullness increased from autumn to a maximum during winter, relating to near‐zero body temperatures which may have effectively stopped gastric evacuation. Although feeding occurred during winter (December to March), consumption rates were calculated as negative values, and subsequently returned to positive values in spring (April to May). The over‐winter life‐history strategy of this sea‐run S. fontinalis population appears to be a feeding marine migration in which fish continually increase body condition, representing an alternative to the more common overwintering strategy of starvation in fresh water until spring.     

Repeatability of individual migration routes,wintering sites,and timing in a long‐distance migrant bird

Migratory birds are often faithful to wintering (nonbreeding) sites, and also migration timing is usually remarkably consistent, that is, highly repeatable. Spatiotemporal repeatability can be of advantage for multiple reasons, including familiarity with local resources and predators as well as avoiding the costs of finding a new place, for example, nesting grounds. However, when the environment is variable in space and time, variable site selection and timing might be more rewarding. To date, studies on spatial and temporal repeatability in short‐lived long‐distance migrants are scarce, most notably of first‐time and subsequent migrations. Here, we investigated repeatability in autumn migration directions, wintering sites, and annual migration timing in Hoopoes (Upupa epops), a long‐distance migrant, using repeated tracks of adult and first‐time migrants. Even though autumn migration directions were mostly the same, individual wintering sites often changed from year to year with distances between wintering sites exceeding 1,000 km. The timing of migration was repeatable within an individual during autumn, but not during spring migration. We suggest that Hoopoes respond to variable environmental conditions such as north–south shifts in rainfall during winter and differing onset of the food availability during spring migration.     

Seasonal migration strategies of Common Ringed Plovers Charadrius hiaticula

How individual birds schedule their movements and use different sites during the non‐breeding season are fundamental issues in avian migration ecology, and studies have often revealed strong seasonal variation in such strategies. Using geolocators we tracked Common Ringed Plovers Charadrius hiaticula from northern Norway to West Africa and back to assess whether there were differences in migratory speed, duration and stopover use between autumn and spring migration and whether birds used multiple sites during the non‐breeding season. Although the pace of migration was similar between autumn and spring, the length of flight bouts and duration of the preceding stopovers were positively correlated only in autumn. Four of five birds showed a marked southward movement in mid‐winter.     

树麻雀代谢率和器官重量在季节驯化中表型的可塑性变化

动物能量代谢的生理生态特征与物种的分布和丰富度密切相关,基础代谢率(BMR)是内温动物能量预算的重要组成部分。北温带的小型鸟类,通过增加产热来适应低温环境。增加BMR的基础之一是中心器官(代谢机器)发生明显的变化。本研究中我们测定了树麻雀(Passermontanus)的BMR、体重和各器官的重量,分析了麻雀各器官的季节性变化及与BMR的关系。方差分析表明:麻雀的BMR存在明显的季节性变化,在冬季和秋季较高。麻雀内部器官的变化同样有明显的季节性,冬季和秋季麻雀的肝脏、心脏、肌胃、小肠、直肠和整体消化道的重量,都有明显的增加。相关分析表明:麻雀的BMR与肝脏、心脏和消化道等内部器官存在明显的相关性。我们的结果验证了“中心限制假说”,即麻雀体内存在着与BMR相关的“代谢机器”,中心器官是提高麻雀BMR的基础之一。     

Annual changes in the concentration of minerals and organic compounds of Quercus suber leaves

Mature leaves are the primary source of sugars, which give rise to many secondary metabolites required for plant survival under adverse conditions. In order to study the interaction of field‐grown cork oak (Quercus suber L.) with the environment, we investigated the seasonal variation of minerals and organic metabolites in the leaves, using inductively coupled plasma atomic emission spectrometry, elemental analysis and nuclear magnetic resonance spectrometry. Statistical analysis showed that the data strongly correlated with seasonal climate and were divided in three groups corresponding to: (1) spring‐early summer, (2) summer and (3) autumn‐winter. The concentration of N, P, K and leaf ash content were highest in spring (recently formed leaves), reached the minimum during the hot and dry summer and increased slightly during the rainy period of autumn‐winter. Conversely, Na, Mg and Ca concentrations were lowest in spring‐early summer and increased during summer and autumn‐winter, the Ca concentration increasing five‐fold. Two cyclitol derivatives, quinic acid and quercitol were the major organic metabolites of the leaves. Their concentration along the season followed opposite trends. While quinic acid predominated during spring‐early summer, when it contributed 12% to the leaf osmotic potential, quercitol was predominant during autumn‐winter, when its contribution to leaf osmotic potential was about 10%. This different preponderance of the two compounds is expressed by the quercitol/quinic acid ratio, which can be as low as 0.2 in early summer and as high as 9 in winter. Sucrose and glucose concentrations also increased during autumn‐winter. Evidence for the quercitol protective role in plants during stress is discussed, and on the basis of structural similarity, it is suggested that quinic acid could have an identical importance, with a protective role against heat and high irradiance. It is concluded that the marked changes in Q. suber leaf composition throughout the year could have important implications in the plant capacity to endure climatic stress.     

Towards a new understanding of migration timing: slower spring than autumn migration in geese reflects different decision rules for stopover use and departure

According to migration theory and several empirical studies, long‐distance migrants are more time‐limited during spring migration and should therefore migrate faster in spring than in autumn. Competition for the best breeding sites is supposed to be the main driver, but timing of migration is often also influenced by environmental factors such as food availability and wind conditions. Using GPS tags, we tracked 65 greater white‐fronted geese Anser albifrons migrating between western Europe and the Russian Arctic during spring and autumn migration over six different years. Contrary to theory, our birds took considerably longer for spring migration (83 days) than autumn migration (42 days). This difference in duration was mainly determined by time spent at stopovers. Timing and space use during migration suggest that the birds were using different strategies in the two seasons: In spring they spread out in a wide front to acquire extra energy stores in many successive stopover sites (to fuel capital breeding), which is in accordance with previous results that white‐fronted geese follow the green wave of spring growth. In autumn they filled up their stores close to the breeding grounds and waited for supportive wind conditions to quickly move to their wintering grounds. Selection for supportive winds was stronger in autumn, when general wind conditions were less favourable than in spring, leading to similar flight speeds in the two seasons. In combination with less stopover time in autumn this led to faster autumn than spring migration. White‐fronted geese thus differ from theory that spring migration is faster than autumn migration. We expect our findings of different decision rules between the two migratory seasons to apply more generally, in particular in large birds in which capital breeding is common, and in birds that meet other environmental conditions along their migration route in autumn than in spring.     

Investigating connectivity and seasonal differences in wind assistance in the migration of Common Sandpipers

Many migratory bird species have undergone recent population declines, but there is considerable variation in trends between species and between populations employing different migratory routes. Understanding species-specific migratory behaviours is therefore of critical importance for their conservation. The Common Sandpiper Actitis hypoleucos is an Afro-Palaearctic migratory bird species whose European populations are in decline. We fitted geolocators to individuals breeding in England or wintering in Senegal to determine their migration routes and breeding or non-breeding locations. We used these geolocator data in combination with previously published data from Scottish breeding birds to determine the distributions and migratory connectivity of breeding (English and Scottish) and wintering (Senegalese) populations of the Common Sandpiper, and used simulated random migrations to investigate wind assistance during autumn and spring migration. We revealed that the Common Sandpipers tagged in England spent the winter in West Africa, and that at least some birds wintering in Senegal bred in Scandinavia; this provides insights into the links between European breeding populations and their wintering grounds. Furthermore, birds tagged in England, Scotland and Senegal overlapped considerably in their migration routes and wintering locations, meaning that local breeding populations could be buffered against habitat change, but susceptible to large-scale environmental changes. These findings also suggest that contrasting population trends in England and Scotland are unlikely to be the result of population-specific migration routes and wintering regions. Finally, we found that birds used wind to facilitate their migration in autumn, but less so in spring, when the wind costs associated with their migrations were higher than expected at random. This was despite the wind costs of simulated migrations being significantly lower in spring than in autumn. Indeed, theory suggests that individuals are under greater time pressures in spring than in autumn because of the time constraints associated with reproduction.