Global climate change and invariable photoperiods: A mismatch that jeopardizes animal fitness

The Earth's surface temperature is rising, and precipitation patterns throughout the Earth are changing; the source of these shifts is likely anthropogenic in nature. Alterations in temperature and precipitation have obvious direct and indirect effects on both plants and animals. Notably, changes in temperature and precipitation alone can have both advantageous and detrimental consequences depending on the species. Typically, production of offspring is timed to coincide with optimal food availability; thus, individuals of many species display annual rhythms of reproductive function. Because it requires substantial time to establish or re‐establish reproductive function, individuals cannot depend on the arrival of seasonal food availability to begin breeding; thus, mechanisms have evolved in many plants and animals to monitor and respond to day length in order to anticipate seasonal changes in the environment. Over evolutionary time, there has been precise fine‐tuning of critical photoperiod and onset/offset of seasonal adaptations. Climate change has provoked changes in the availability of insects and plants which shifts the timing of optimal reproduction. However, adaptations to the stable photoperiod may be insufficiently plastic to allow a shift in the seasonal timing of bird and mammal breeding. Coupled with the effects of light pollution which prevents these species from determining day length, climate change presents extreme evolutionary pressure that can result in severe deleterious consequences for individual species reproduction and survival. This review describes the effects of climate change on plants and animals, defines photoperiod and the physiological events it regulates, and addresses the consequences of global climate change and a stable photoperiod.     

Cold adaptation in marine organisms

Animals from polar seas exhibit numerous so called resistance adaptations that serve to maintain homeostasis at low temperature and prevent lethal freezing injury. Specialization to temperatures at or below 0 degrees C is associated with an inability to survive at temperatures above 3-8 degrees C. Polar fish synthesize various types of glycoproteins or peptides to lower the freezing point of most extracellular fluid compartments in a non-colligative manner. Antifreeze production is seasonal in boreal species and is often initiated by environmental cues other than low temperature, particularly short day lengths. Most of the adaptations that enable intertidal invertebrates to survive freezing are associated with their ability to withstand ariel exposure. Unique adaptations for freezing avoidance include the synthesis of low molecular mass ice-nucleating proteins that control and induce extracellular ice-formation. Marine poikilotherms also exhibit a range of capacity adaptations that increase the rate of some physiological processes so as to partially compensate for the effects of low temperature. However, the rate of embryonic development in a diverse range of marine organisms shows no evidence of temperature compensation. This results in a significant lengthening of the time from fertilization to hatching in polar, relative to temperate, species. Some aspects of the physiology of polar marine species, such as low metabolic and slow growth rates, probably result from a combination of low temperature and other factors such as the highly seasonal nature of food supplies. Although neuromuscular function shows a partial capacity adaptation in Antarctic fish, maximum swimming speeds are lower than for temperate and tropical species, particularly for early stages in the life history.     

Adaptation of mammalian host-pathogen interactions in a changing arctic environment

Many arctic mammals are adapted to live year-round in extreme environments with low winter temperatures and great seasonal variations in key variables (e.g. sunlight, food, temperature, moisture). The interaction between hosts and pathogens in high northern latitudes is not very well understood with respect to intra-annual cycles (seasons). The annual cycles of interacting pathogen and host biology is regulated in part by highly synchronized temperature and photoperiod changes during seasonal transitions (e.g., freezeup and breakup). With a warming climate, only one of these key biological cues will undergo drastic changes, while the other will remain fixed. This uncoupling can theoretically have drastic consequences on host-pathogen interactions. These poorly understood cues together with a changing climate by itself will challenge host populations that are adapted to pathogens under the historic and current climate regime. We will review adaptations of both host and pathogens to the extreme conditions at high latitudes and explore some potential consequences of rapid changes in the Arctic.     

Hydrostatic Pressure and Temperature Effects on the Membranes of a Seasonally Migrating Marine Copepod

Marine planktonic copepods of the order Calanoida are central to the ecology and productivity of high latitude ecosystems, representing the interface between primary producers and fish. These animals typically undertake a seasonal vertical migration into the deep sea, where they remain dormant for periods of between three and nine months. Descending copepods are subject to low temperatures and increased hydrostatic pressures. Nothing is known about how these organisms adapt their membranes to these environmental stressors. We collected copepods (Calanoides acutus) from the Southern Ocean at depth horizons ranging from surface waters down to 1000 m. Temperature and/or pressure both had significant, additive effects on the overall composition of the membrane phospholipid fatty acids (PLFAs) in C. acutus. The most prominent constituent of the PLFAs, the polyunsaturated fatty acid docosahexanoic acid [DHA – 22:6(n-3)], was affected by a significant interaction between temperature and pressure. This moiety increased with pressure, with the rate of increase being greater at colder temperatures. We suggest that DHA is key to the physiological adaptations of vertically migrating zooplankton, most likely because the biophysical properties of this compound are suited to maintaining membrane order in the cold, high pressure conditions that persist in the deep sea. As copepods cannot synthesise DHA and do not feed during dormancy, sufficient DHA must be accumulated through ingestion before migration is initiated. Climate-driven changes in the timing and abundance of the flagellated microplankton that supply DHA to copepods have major implications for the capacity of these animals to undertake their seasonal life cycle successfully.     

Pressure-regulated metabolism in microorganisms.

There has been a renewal of interest in the survival strategies employed by deep-sea, high-pressure-adapted (piezophilic) microorganisms as well as in the effects of high pressure on mesophilic, 1-atmosphere-pressure-adapted microorganisms. This is partly the result of a greater appreciation of the adaptations of microorganisms to life in extreme environments and partly the result of the development of new techniques for examining physiological and molecular processes as a function of pressure.     

Responses of the killifish (Aphanius dispar) to long-term exposure to elevated temperatures: growth,survival and microstructure of gill and heart tissues

Some fish species, such as killifish, that normally inhabit temperate water environments are also found in extreme thermal environments such as thermal springs. The extent of the adaptations involved is not known. In the present laboratory study, we exposed killifish (Aphanius dispar) acclimated to a normal thermal environment to elevated temperatures (37–40 °C) in which related killifish species live permanently. Our objective was to determine whether there is evidence that killifish have heat-shock characteristics that make permanent adaptation likely. The fish was exposed to this temperature for a period of 44 days and then compared with control fish kept at their normal temperature (24 °C) with respect to growth, survival and histopathology of gill and heart tissues. At the end of the experimental time, the percentage of body weight gain and specific growth rate were significantly lower in fish kept in thermal stress compared with the control group. Feed conversion ratio (FCR) was also significantly affected by water temperature, so that during thermal stress the values of FCR were negative. Fish condition (Condition factor: CF) did not differ significantly between both groups at the end of the experiment. On days 11 and 33, however, CF was significantly lower in the thermal stress group. The gill showed blood congestion in primary lamellae and shortened secondary lamellae in fish kept at 37–40 °C. No specific alterations were found in the cardiac tissue of fish kept in thermal stress conditions. Under thermal stress, 40% of fish survived until the end of the experiment. A preliminary conclusion drawn from this work is that A. dispar, which lives at normal temperatures, shows evidence of adaptability to elevated temperatures that could be a factor in the ability of killifish to adapt permanently over time to thermal environment.     

Oxygen transport in extreme environments.

Evolution has adopted different strategies to solve the problem of transporting oxygen to respiring tissues, according to needs dictated by the environment. A thermodynamic analysis of haemoglobins of organisms living in extreme polar environments (mammals and fish) provides elegant examples of such adaptations.     

Seasonality of reproduction and production in farm fishes, birds and mammals

A very large majority of farm animals express seasonal variations in their production traits, thus inducing seasonal availability of fresh derived animal products (meat, milk, cheese and eggs). This pattern is in part the consequence of the farmer's objective to market his products in the most economically favourable period. It may also be imposed by the season-dependent access to feed resources, as in ruminants, or by the specific requirements derived from adaptation to environmental conditions such as water temperature in fish. But seasonal variations in animal products are also the consequence of constraints resulting from the occurrence of a more or less marked seasonal reproductive season in most farm animal species including fish, poultry and mammals. Like their wild counterparts, at mid and high latitudes, most farm animals normally give birth at the end of winter-early spring, the most favourable period for the progeny to survive and thus promote the next generation. As a consequence, most species show seasonal variations in their ovulation frequency (mammals and fish: presence or absence of ovulation; birds: variations or suppression of laying rates), spermatogenic activity (from moderate to complete absence of sperm production), gamete quality (variations in fertilisation rates and embryo survival), and also sexual behaviour. Among species of interest for animal production, fishes and birds are generally considered as more directly sensitive to external factors (mainly temperature in fish, photoperiod in birds). In all species, it is therefore advisable that artificial photoperiodic treatments consisting of extra-light during natural short days (in chickens, turkeys, guinea fowl, sheep and goats) or melatonin during long days (in goats, sheep) be extensively used to either adjust the breeding season to animal producer needs and/or to completely overcome seasonal variations of sperm production in artificial insemination centres (mammals) and breeder flock operations (poultry, fish farming). Pure light treatments (without melatonin), especially when applied in open barns, could be considered as non invasive ones which fully respect animal welfare.     

Physiological effects of dominance hierarchies: laboratory artefacts or natural phenomena?

Studies of fish behaviour have demonstrated the existence of social interactions that result in dominance hierarchies. In environments in which resources, such as food, shelter and mates, are limited, social competition results in some fish becoming dominant and occupying the most profitable positions. This behaviour has been observed in natural environments and also in many laboratory‐based experiments. When two fish have been confined in a small tank, one of them usually has exhibited behaviour that suggests it is dominant over the other submissive animal. Physiological consequences of social interaction can be seen in both dominants and subordinates but are more extreme in the subordinate. However, this scenario is without doubt an artificial situation. Fewer experiments have been conducted using laboratory experiments that are more socially and physically complex than those experienced by dyads in tanks. In simple fluvial tanks, through which water is recirculated, the physiological responses of fish to social competition have generally been qualitatively similar to those recorded among dyads. However, when environmental disturbances, complex resource distributions, increase in water flushing, presence of predators and competing species of fish have been included in experimen‐tal designs, there have been fewer, diminished or no physiological dierences between dominant and subordinate fish. There have been very few studies of physiology in relation to dominance in natural habitats, and those that have been conducted suggest that under some circumstances hierarchies may cause less intense physiological responses than have been suggested based on results of laboratory studies in simple environments. Possible reasons for these variations are discussed. The need is identified for a well structured experimental approach to the investi‐gation of the causes and consequences of hierarchies if the ecology of wild fish is to be modelled eectively based on physiological processes. It is also suggested that the further development and application of techniques for monitoring physiologies of fish in the wild is important.     

Seed structure and germination in buriti (Mauritia flexuosa), the Swamp palm

Associations of recalcitrance and dormancy are rare, and little information is available concerning the structure of seeds demonstrating this type of behavior or their ecological implications. Mauritia flexuosa is a palm tree associated with swampy environments in the Amazon rainforest and areas of Cerrado (neotropical savanna), the latter biome having marked climatic seasonality. We describe the structures and physiological aspects of the seeds and seedlings of this species to examine its adaptations to swampy environments and its germination control mechanisms, as well as the relationship between recalcitrance and dormancy in terms of reproductive success. Morphoanatomy and histochemistry of the seeds and seedlings were evaluated using standard methodologies, and the effects of temperature and operculum removal on germination were investigated. Differentiated tracheal elements in the embryo are associated with recalcitrance, and presence of numerous stomata on the embryo and the abundance of secondary metabolite compounds in the seedling indicate their adaptations to swampy environments. The inability of the embryo to overcome the resistance of the adjacent tissues determines dormancy of the physiological type, thus the removal of the operculum is an efficient method for promoting propagation. Cellular elongation in the cotyledon promotes seedling protrusion. Mobilization of endosperm reserves is achieved by symplastic flux and is associated with overcoming of dormancy by weakening the tissues adjacent to the embryo. The association between recalcitrance, which favors adaptation to swampy environments, and dormancy, which favors dispersal, is crucial for the reproductive success of this species and its broad geographical distribution.     

Culturability and Secondary Metabolite Diversity of Extreme Microbes: Expanding Contribution of Deep Sea and Deep-Sea Vent Microbes to Natural Product Discovery

Microbes from extreme environments do not necessarily require extreme culture conditions. Perhaps the most extreme environments known, deep-sea hydrothermal vent sites, support an incredible array of archaea, bacteria, and fungi, many of which have now been cultured. Microbes cultured from extreme environments have not disappointed in the natural products arena; diverse bioactive secondary metabolites have been isolated from cultured extreme-tolerant microbes, extremophiles, and deep-sea microbes. The contribution of vent microbes to our arsenal of natural products will likely grow, given the culturability of vent microbes; their metabolic, physiologic, and phylogenetic diversity; numerous reports of bioactive natural products from microbes inhabiting high acid, high temperature, or high pressure environments; and the recent isolation of new chroman derivatives and siderophores from deep-sea hydrothermal vent bacteria.     

Organisms of deep sea hydrothermal vents as a source for studying adaptation and evolution

It has been postulated that life originated in a similar environment to those of deep sea hydrothermal vents. These environments are located along volcanic ridges and are characterized by extreme conditions such as unique physical properties (temperature, pressure), chemical toxicity, and absence of photosynthesis. However, numerous living organisms have been discovered in these hostile environments, including a variety of microorganisms and many animal species which live in intimate and complex symbioses with sulfo-oxidizing and methanotrophic bacteria. Recent proteomic analyses of the endosymbiont ofRiftia pachyptila and genome sequences of some free living and symbiotic bacteria have provided complementary information about the potential metabolic and genomic capacities of these organisms. The evolution of these adaptive strategies is connected with different mechanisms of genetic adaptation including horizontal gene transfer and . various structural and functional mutations. Therefore, the organisms in this environment are good models for studying the evolution of prokaryotes and eukaryotes as well as different aspects of the biology of adaptation. This review describes some current research concerning metabolic and plausible genetic adaptations of organisms in a deep sea environment, usingRiftia pachyptila as model.     

Seasonal variation in reef fish assemblages in the environmentally extreme southern Persian/Arabian Gulf

The southern Persian/Arabian Gulf experiences extreme seasonal temperature variation (> 20 °C) making it among the most hostile reef environments on Earth. Previous anecdotal evidence has suggested that seasonal temperature changes may influence regional reef fish assemblages, but to date research has been limited. To examine the influence of temperature on reef fish abundance and composition, we performed visual surveys in summer and in winter over three years at three reefs in the southern Gulf (Dhabiya, Saadiyat and Ras Ghanada). Overall abundance of fishes was 40% higher in summer than in winter, and multivariate analyses showed strong and significant differences in overall seasonal community structure, consistent at all sites and across all years. Seasonal differences were largely driven by nine of the 30 observed species, which together accounted for 70% of the divergence in community structure between summer and winter. Of these nine species, Lutjanus ehrenbergii, Lutjanus fulviflamma, Plectorhinchus sordidus and Abudefduf vaigiensis were significantly more abundant in summer, Parupeneus margaritatus and Acanthopagrus bifasciatus, were significantly more common on reefs in winter. We discuss these changes in terms of seasonal physiological and ecological constraints, and explore the implications of these changes on the functional ecology of reef fishes in this thermally variable and extreme environment.

     

Circannual variation in habitat use of the White-winged Snowfinch Montifringilla nivalis nivalis

High mountain areas are subject to strong seasonal fluctuations, and species inhabiting these particular environments show a high degree of habitat specialization to cope with extreme abiotic conditions. Estimates of habitat use are influenced by the spatial and seasonal scales at which they are evaluated, so studies at multiple scales are important in order to explore adaptive responses to seasonal environments. In the present study, we assessed habitat use of the White-winged Snowfinch Montifringilla nivalis subsp. nivalis (henceforth Snowfinch) during breeding and non-breeding seasons at three different spatial scales (diameters of 100, 250 and 500 m). Although Snowfinches clearly used high-elevation habitats in both seasons, there was evidence that they are less specific during the non-breeding period: the variance explained by habitat and topographical factors was lower in winter than in the breeding season. Moreover, our results suggest that the use of habitat is scale-dependent. This pattern was especially relevant in the breeding season, perhaps because habitat use might be more related to nest-site selection and specific foraging sites to provide food for nestlings. Snowfinches use high mountain habitats throughout the year, probably as a consequence of physiological and morphological specializations typical of high-elevation species, but in winter they show a certain flexibility in habitat use. Snowfinches might thus adopt a flexible specialist strategy. This could represent a trade-off to overcome possible effects on survival, condition and fitness, which can be particularly strong in harsh, unpredictable environments.     

Effects of temperature and pressure on the lateral organization of model membranes with functionally reconstituted multidrug transporter LmrA

To contribute to the understanding of membrane protein function upon application of pressure, we investigated the influence of hydrostatic pressure on the conformational order and phase behavior of the multidrug transporter LmrA in biomembrane systems. To this end, the membrane protein was reconstituted into various lipid bilayer systems of different chain length, conformation, phase state and heterogeneity, including raft model mixtures as well as some natural lipid extracts. In the first step, we determined the temperature stability of the protein itself and verified its reconstitution into the lipid bilayer systems using CD spectroscopic and AFM measurements, respectively. Then, to yield information on the temperature and pressure dependent conformation and phase state of the lipid bilayer systems, generalized polarization values by the Laurdan fluorescence technique were determined, which report on the conformation and phase state of the lipid bilayer system. The temperature-dependent measurements were carried out in the temperature range 5-70 °C, and the pressure dependent measurements were performed in the range 1-200 MPa. The data show that the effect of the LmrA reconstitution on the conformation and phase state of the lipid matrix depends on the fluidity and hydrophobic matching conditions of the lipid system. The effect is most pronounced for fluid DMPC and DMPC with low cholesterol levels, but minor for longer-chain fluid phospholipids such as DOPC and model raft mixtures such as DOPC/DPPC/cholesterol. The latter have the additional advantage of using lipid sorting to avoid substantial hydrophobic mismatch. Notably, the most drastic effect was observed for the neutral/glycolipid natural lipid mixture. In this case, the impact of LmrA incorporation on the increase of the conformational order of the lipid membrane was most pronounced. As a consequence, the membrane reaches a mechanical stability which makes it very insensitive to application of pressures as high as 200 MPa. The results are correlated with the functional properties of LmrA in these various lipid environments and upon application of high hydrostatic pressure and are discussed in the context of other work on pressure effects on membrane protein systems.     

Morphologically Conservative but Physiologically Diverse: The Mode of Stasis in Anostraca (Crustacea: Branchiopoda)

The essay discusses whether biotic and abiotic environments differ in their ability to speed up or slow down morphological change and the generation of new lineages. Examples from the class Branchiopoda show that morphological conservatism is associated with enemy free space in species-poor habitats dominated by abiotic factors, while Red Queen mechanisms are predominant in larger systems with complex biotic interactions. Splitting of Branchiopod main lineages is associated with increased fish predation during the Devonian. The order Cladocera adapted and remained in larger aquatic systems, and subsequently generated a variety of new families, genera and species. The order Anostraca, on the other hand, maintained its ancestral morphology and survived only as “living fossils” in isolated ponds of harsh habitats. Despite their archaic morphology, however, they possess highly sophisticated adaptations to local physicochemical properties of their extreme environment. Hence, although morphologically conservative and possessing traits typical for “living fossils”, anostracan physiological abilities are closely adapted to the challenging and variable physicochemical conditions of ponds and ephemeral pools.     

Adaptations of fish species to oxygen depletion in a central Amazonian floodplain lake

Pronounced seasonal and daily oxygen concentration changes are characteristic for Amazonian floodplain lakes. Studies on the fish fauna of the Lago Camaleão, Solimões River, Amazonas, Brazil, showed several fish species which are able to survive prolonged periods of heavy hypoxia. Twenty species belonging to eight families were observed in the laboratory in order to determine their respiratory adaptations to hypoxic conditions and oxygen concentrations at which the fish present respiratory adaptations. Finally, the fish species were distributed throughout the habitats of Lake Camaleão according to their adaptation responses. Ten fish species used the surface water for aquatic surface respiration, four species used atmospheric oxygen for aerial respiration, four species used oxygen supplied by the exudation of the roots of floating macrophytes and two exhibited a high tolerance to hypoxic conditions, and well-developed physiological biochemical mechanisms. The fish fauna is well adapted to low oxygen concentrations. The large variety of morpho-anatomical adaptations associated with biochemical and physiological mechanisms to tolerate hypoxic and anoxic conditions enable the 20 fish species to exploit several habitats of Lago Camaleão, such as floating aquatic macrophyte meadows, open water and near the shoreline.     

Linkages among physical and biological properties in tidepools on the Maine Coast

Tidepools experience significant gradients in ecologically relevant physical variables along the transition from ocean to terrestrial habitat (vertical axis) and from open coast to inner bays (horizontal axis). Associations amongst physical and biological variables, divided into algal, invertebrate and vertebrate (fish) groups, were examined in a tidepool survey dataset. Physical variables and the three biological groups were submitted separately to a principal component analysis (PCA). PCA scores were evaluated with Pearson correlation coefficients across the sampling units (tidepools) to identify significant correlations. Initially little structure in the data and no correlation amongst variables was present. At the onset of summer, correlations were confined amongst physical variables and algal and invertebrate components, followed in the late summer with correlations between invertebrate and fish components. By the fall, correlations were confined to fish and algal/invertebrate components. Species relationships followed a seasonal cycle with a succession from little to no structure, the forming of low trophic level relationships in the early summer to high trophic level relationships in late summer-fall, and deconstruction of structure with the onset of fall-winter storms and ice scour. The seasonal pattern, and well established vertical gradient, has nested within it species composition changes along a horizontal wave energy gradient. The horizontal gradient results in a shift from species which are physiologically adapted to extreme salinities and temperatures to those which are physically adapted to high wave-energy environments.     

Predation pressure induced by seasonal fishing moratorium changes the dynamics of subtropical Cladocera populations

Seasonal fishing moratorium with selective fish harvesting is a common means of increasing fish production in Asia. Such manipulation might be expected to lead to a seasonal variation in abundance and composition of fish and predation pressure on zooplankton, and consequently a seasonal change in the Cladocera populations. In this study, we examined the seasonal dynamics of cladocerans in a subtropical plateau lake in southwestern China, Lake Erh, in which a fishing moratorium was implemented in spring and early summer. Cladocerans showed a bimodal seasonal distribution linked to variations in predation pressure induced by the seasonal fishing moratorium. When predation was low in winter because of cool water temperatures and decreasing fish density, Daphnia galeata appeared in the water column and increased towards spring. The cladoceran peaked in the middle of the fishing moratorium, coinciding with a clear water phase. The feeding rate increased with temperature in the late moratorium, allowing planktivorous fish to strongly suppress large daphnids. Small cladocerans benefited from the reduced competition with large daphnids by increasing their numbers rapidly, which resulted in a second peak of cladocerans in the fishing season.