A perspective on insect–microbe holobionts facing thermal fluctuations in a climate-change context

Temperature influences the ecology and evolution of insects and their symbionts by impacting each partner independently and their interactions, considering the holobiont as a primary unit of selection. There are sound data about the responses of these partnerships to constant temperatures and sporadic thermal stress (mostly heat shock). However, the current understanding of the thermal ecology of insect–microbe holobionts remains patchy because the complex thermal fluctuations (at different spatial and temporal scales) experienced by these organisms in nature have often been overlooked experimentally. This may drastically constrain our ability to predict the fate of mutualistic interactions under climate change, which will alter both mean temperatures and thermal variability. Here, we tackle down these issues by focusing on the effects of temperature fluctuations on the evolutionary ecology of insect–microbe holobionts. We propose potentially worth-investigating research avenues to (i) evaluate the relevance of theoretical concepts used to predict the biological impacts of temperature fluctuations when applied to holobionts; (ii) acknowledge the plastic (behavioural thermoregulation, physiological acclimation) and genetic responses (evolution) expressed by holobionts in fluctuating thermal environments; and (iii) explore the potential impacts of previously unconsidered patterns of temperature fluctuations on the outcomes and the dynamic of these insect–microbe associations.     

Influences of thermal environment on fish growth

Thermoregulation in ectothermic animals is influenced by the ability to effectively respond to thermal variations. While it is known that ectotherms are affected by thermal changes, it remains unknown whether physiological and/or metabolic traits are impacted by modifications to the thermal environment. Our research provides key evidence that fish ectotherms are highly influenced by thermal variability during development, which leads to important modifications at several metabolic levels (e.g., growth trajectories, microstructural alterations, muscle injuries, and molecular mechanisms). In Atlantic salmon (Salmo salar), a wide thermal range (Δ_T 6.4°C) during development (posthatch larvae to juveniles) was associated with increases in key thermal performance measures for survival and growth trajectory. Other metabolic traits were also significantly influenced, such as size, muscle cellularity, and molecular growth regulators possibly affected by adaptive processes. In contrast, a restricted thermal range (Δ_T 1.4°C) was detrimental to growth, survival, and cellular microstructure as muscle growth could not keep pace with increased metabolic demands. These findings provide a possible basic explanation for the effects of thermal environment during growth. In conclusion, our results highlight the key role of thermal range amplitude on survival and on interactions with major metabolism‐regulating processes that have positive adaptive effects for organisms.     

Thermal tolerance of the crab Pachygrapsus marmoratus: intraspecific differences at a physiological (CTMax) and molecular level (Hsp70)

Temperature is one of the most important variables influencing organisms, especially in the intertidal zone. This work aimed to test physiological and molecular intraspecific differences in thermal tolerance of the crab Pachygrapsus marmoratus (Fabricius, 1787). The comparisons made focused on sex, size, and habitat (estuary and coast) differences. The physiological parameter was upper thermal limit, tested via the critical thermal maximum (CTMax) and the molecular parameter was total heat shock protein 70 (Hsp70 and Hsp70 plus Hsc70) production, quantified via an enzyme-linked imunosorbent assay. Results showed that CTMax values and Hsp70 production are higher in females probably due to different microhabitat use and potentially due to different hormonal regulation in males and females. Among females, non-reproducing ones showed a higher CTMax value, but no differences were found in Hsp70, even though reproducing females showed higher variability in Hsp70 amounts. As reproduction takes up a lot of energy, its allocation for other activities, including stress responses, is lower. Juveniles also showed higher CTMax and Hsp70 expression because they occur in greater shore heights and ageing leads to alterations in protein synthesis. Comparing estuarine and coastal crabs, no differences were found in CTMax but coastal crabs produce more Hsp70 than estuarine crabs because they occur in drier and hotter areas than estuarine ones, which occur in moister environments. This work shows the importance of addressing intraspecific differences in the stress response at different organizational levels. This study shows that these differences are key factors in stress research, climate research, and environmental monitoring.     

Physiological ecology meets climate change

In this article, we pointed out that understanding the physiology of differential climate change effects on organisms is one of the many urgent challenges faced in ecology and evolutionary biology. We explore how physiological ecology can contribute to a holistic view of climate change impacts on organisms and ecosystems and their evolutionary responses. We suggest that theoretical and experimental efforts not only need to improve our understanding of thermal limits to organisms, but also to consider multiple stressors both on land and in the oceans. As an example, we discuss recent efforts to understand the effects of various global change drivers on aquatic ectotherms in the field that led to the development of the concept of oxygen and capacity limited thermal tolerance (OCLTT) as a framework integrating various drivers and linking organisational levels from ecosystem to organism, tissue, cell, and molecules. We suggest seven core objectives of a comprehensive research program comprising the interplay among physiological, ecological, and evolutionary approaches for both aquatic and terrestrial organisms. While studies of individual aspects are already underway in many laboratories worldwide, integration of these findings into conceptual frameworks is needed not only within one organism group such as animals but also across organism domains such as Archaea, Bacteria, and Eukarya. Indeed, development of unifying concepts is relevant for interpreting existing and future findings in a coherent way and for projecting the future ecological and evolutionary effects of climate change on functional biodiversity. We also suggest that OCLTT may in the end and from an evolutionary point of view, be able to explain the limited thermal tolerance of metazoans when compared to other organisms.     

A study on body temperature regulation and residential thermal environments of the elderly—I. whole country survey of residential thermal environment and evaluation methods: RTE-index

1. 1. As part of “research on environmental comfort,” that is, research which aims to make people's living environment more comfortable, we attempted to clarify the relation between the living environment of elderly people and physiological and psychological factors. We carried out a comprehensive study with a view to establishing comfort standards for the residential thermal environment, and for creating evaluation and control systems.

2. 2. The comfort of the living environment is closely related to the thermal environment and the temperature-regulation ability of the human body. This ability of the body to regulate temperature develops during childhood and recedes as the adult ages.

3. 3. We therefore carried out: (a) experiments on body-temperature regulation and on special characteristics of the body-temperature regulation of elderly people, (b) a nationwide survey of the actual residential thermal environments of elderly people and (c) a survey of the daily activities of elderly people, and how elderly people's physiological and psychological conditions change when they are engaged in these activities.

4. 4. As a result of these experiments and surveys, we were able to: (d) formulate standards for evaluation of the residential thermal environment and (e) numerically express the results of systematic evaluation of residential thermal environments of elderly people, by means of a RTE-index.

Cyclic variations in incubation conditions induce adaptive responses to later heat exposure in chickens: a review

Selection programs have enabled broiler chickens to gain muscle mass without similar enlargement of the cardiovascular and respiratory systems that are essential for thermoregulatory efficiency. Meat-type chickens cope with high ambient temperature by reducing feed intake and growth during chronic and moderate heat exposure. In case of acute heat exposure, a dramatic increase in morbidity and mortality can occur. In order to alleviate heat stress in the long term, research has recently focused on early thermal manipulation. Aimed at stimulation of long-term thermotolerance, the thermal manipulation of embryos is a method based on fine tuning of incubation conditions, taking into account the level and duration of increases in temperature and relative humidity during a critical period of embryogenesis. The consequences of thermal manipulation on the performance and meat quality of broiler chickens have been explored to ensure the potential application of this strategy. The physiological basis of the method is the induction of epigenetic and metabolic mechanisms that control body temperature in the long term. Early thermal manipulation can enhance poultry resistance to environmental changes without much effect on growth performance. This review presents the main strategies of early heat exposure and the physiological concepts on which these methods were based. The cellular mechanisms potentially underlying the adaptive response are discussed as well as the potential interest of thermal manipulation of embryos for poultry production.     

Synergistic and Antagonistic Effects of Thermal Shock,Air Exposure,and Fishing Capture on the Physiological Stress of Squilla mantis (Stomatopoda)

This study is aimed at assessing the effects of multiple stressors (thermal shock, fishing capture, and exposure to air) on the benthic stomatopod Squilla mantis, a burrowing crustacean quite widespread in the Mediterranean Sea. Laboratory analyses were carried out to explore the physiological impairment onset over time, based on emersion and thermal shocks, on farmed individuals. Parallel field-based studies were carried out to also investigate the role of fishing (i.e., otter trawling) in inducing physiological imbalance in different seasonal conditions. The dynamics of physiological recovery from physiological disruption were also studied. Physiological stress was assessed by analysing hemolymph metabolites (L-Lactate, D-glucose, ammonia, and H⁺), as well as glycogen concentration in muscle tissues. The experiments were carried out according to a factorial scheme considering the three factors (thermal shock, fishing capture, and exposure to air) at two fixed levels in order to explore possible synergistic, additive, or antagonistic effects among factors. Additive effects on physiological parameters were mainly detected when the three factors interacted together while synergistic effects were found as effect of the combination of two factors. This finding highlights that the physiological adaptive and maladaptive processes induced by the stressors result in a dynamic response that may encounter physiological limits when high stress levels are sustained. Thus, a further increase in the physiological parameters due to synergies cannot be reached. Moreover, when critical limits are encountered, mortality occurs and physiological parameters reflect the response of the last survivors. In the light of our mortality studies, thermal shock and exposure to air have the main effect on the survival of S. mantis only on trawled individuals, while lab-farmed individuals did not show any mortality during exposure to air until after 2 hours.     

Repeated thermal stressor causes chronic elevation of baseline corticosterone and suppresses the physiological endocrine sensitivity to acute stressor in the cane toad (Rhinella marina)

Extreme environmental temperature could impact the physiology and ecology of animals. The stress endocrine axis provides necessary physiological stress response to acute (day–day) stressors. Presently, there are no empirical evidences showing that exposure to extreme thermal stressor could cause chronic stress in amphibians. This could also modulate the physiological endocrine sensitivity to acute stressors and have serious implications for stress coping in amphibians, particularly those living in fragmented and disease prone environments. We addressed this important question using the cane toad (Rhinella marina) model from its introduced range in Queensland, Australia. We quantified their physiological endocrine sensitivity to a standard acute (capture and handling) stressor after exposing the cane toads to thermal shock at 35 °C for 30 min daily for 34 days. Corticosterone (CORT) responses to the capture and handling protocol were measured on three sampling intervals (days 14, 24, and 34) to determine whether the physiological endocrine sensitivity was maintained or modulated over-time. Two control groups (C1 for baseline CORT measurement only and C2 acute handled only) and two temperature treatment groups (T1 received daily thermal shock up to day 14 only and a recovery phase of 20 days and T2 received thermal shock daily for 34 days). Results showed that baseline CORT levels remained high on day 14 (combined effect of capture, captivity and thermal stress) for both T1 and T2. Furthermore, baseline CORT levels decreased for T1 once the thermal shock was removed after day 14 and returned to baseline by day 29. On the contrary, baseline CORT levels kept on increasing for T2 over the 34 days of daily thermal shocks. Furthermore, the magnitudes of the acute CORT responses or physiological endocrine sensitivity were consistently high for both C1 and T1. However, acute CORT responses for T2 toads were dramatically reduced between days 24 and 34. These novel findings suggest that repeated exposure to extreme thermal stressor could cause chronic stress and consequently suppress the physiological endocrine sensitivity to acute stressors (e.g. pathogenic diseases) in amphibians.     

Evaluating cognition and thermal physiology as components of the pace-of-life syndrome

The pace-of-life syndrome (POLS) suggests that behavioral traits are correlated and integrate within a fast–slow physiological continuum. At the fast extreme, individuals having higher metabolic rates are more active, exploratory, and bold with the opposite suite of traits characterizing those at the slow physiological extreme. A recent framework suggests that behavioral types may also differ consistently in their cognitive style. Accordingly, we propose that cognition could be further incorporated into the POLS framework comprised of behavioral and thermal physiological traits. Under this premise, fast behavioral types having high thermal traits are predicted to acquire a novel task faster but at the cost of accuracy while slow behavioral types with low thermal traits would be more attentive, responding to cues at a slower rate leading to higher accuracy and flexibility. This was tested by measuring physiological and behavioral traits in delicate skinks (Lampropholis delicata) and testing their learning ability. Correlations were detected between cognition and behavior but not thermal physiology. Contrary to our predictions, individual positioning along these axes opposed our predicted directions along the fast–slow continuum. Fast lizards preferring lower body temperatures expressed higher activity, exploration, sociality, and boldness levels, and learned the discrimination learning task at a slower rate but made the most errors. Additionally, modelling results indicated that neither thermal physiology, behavior, or their interaction influenced cognitive performance. Although the small number of animals completing the final stages of the learning assays limits the strength of these findings. Thus, we propose that future research involving a greater sample size and number of trials be conducted so as to enhance our understanding into how the integration of cognitive style, behavior, and physiology may influence individual fitness within natural populations.     

Repeatability and correlation of physiological traits: Do ectotherms have a “thermal type”?

Across a range of taxa, individuals within a species differ in suites of correlated traits. These trait complexes, known as syndromes, can have dramatic evolutionary consequences as they do not evolve independently but rather as a unit. Current research focuses primarily on syndromes relating to aspects of behavior and life history. What is less clear is whether physiological traits also form a syndrome. We measured 10 thermal traits in the delicate skink, Lampropholis delicata, to test this idea. Repeatability was calculated and their across‐context correlations evaluated. Our results were in alignment with our predictions in that individual thermal traits varied consistently and were structured into a physiological syndrome, which we are referring to as the thermal behavior syndrome (TBS). Within this syndrome, lizards exhibited a “thermal type” with each being ranked along a cold–hot continuum. Hot types had faster sprint speeds and higher preferred body temperatures, whereas the opposite was true for cold types. We conclude that physiological traits may evolve as a single unit driven by the need to maintain optimal temperatures that enable fitness‐related behaviors to be maximized.     

Hsp70 is not a sensitive indicator of thermal limitation in Gadus morhua

The levels of heat‐shock proteins of the 70 kDa family (Hsp70s) were measured in different soft tissues of Atlantic cod Gadus morhua from different locations and after exposure to various thermal conditions: acute temperature increments (1° C day⁻¹), mid‐term (73 days at 4–15° C) and long‐term thermal acclimation (278 days at 8–15° C), and seasonal and latitudinal temperature variations (field samples). Tissue specific distribution patterns of Hsp70s were observed: liver > gills > red blood cells > brain > white muscle. Thus, different tissues may have required different levels of protection by Hsp70s, and possibly this was related to the rate of protein synthesis. There were no differences in tissue Hsp70s between Arctic cod populations (Arctic, i.e . Barents and White Seas, Norwegian coast, and North or Baltic Seas). No changes in Hsp70s levels were observed in response to temperature variation of any intensity (acute fluctuation or seasonal and latitudinal) within the range of physiological temperatures (4–15° C) in wild and laboratory Atlantic cod. This confirms previous observations that changes in Hsp70 caused by such temperature variation are often small in fishes. Probably, the constitutive level of Hsp70s in Atlantic cod was high enough to overcome potentially harmful effects of temperature variations within the physiological range. A suppressing effect of high temperature (15° C) has already been observed at a systematic level (as reduced rate of somatic growth), whereas it is not reflected in modified Hsp70s. Therefore, Hsp70s apparently played a secondary role in defining thermal tolerance limits in Atlantic cod. These conclusions are in line with a recent concept of thermal tolerance which indicated that the first line of thermal limitation in the cold and warm is a loss in aerobic scope.     

Temperature studies and recent advances with fish cells in vitro

Understanding how fish respond to a changing thermal environment requires research at multiple levels, from molecular to ecological. Piscine cell culturing is a relatively new approach for studies at the cellular level and could be particularly valuable for integrating molecular and physiological studies. Improvements in culturing and genetically modifying piscine cells in vitro should increase the value of this approach.     

Plant clonality: Biology and diversity

The current approaches to the study of clonal plants are reviewed. Most studies concentrate at the level of the ramet and clonal fragment exploring the “microscopic” view of clonal plants, dealing with the translocation of resources, clonal integration, plasticity of growth etc. The information gained, by this approach can be used in the understanding of higher levels of organization within the clonal system either with the help of spatially explicit modelling techniques, or by using means and distributions of size within a population instead of studying individual ramets separately. Plant scientists use the term clone with two meanings, viz. (a) a set of physiologically connected, but potentially independent ramets, and (b) a set of genetically identical, but potentially physically separated individuals. The overlap of these terms differs between individual plant species, depending on the extent of physical separation of the ramets and the degree of physiological integration between the ramets; the lower the frequency of ramet separation, the closer are the physiological and genetic concepts of the clone. Three critical areas seem to be neglected in clonal plant research: (a) the interrelationship between hierarchical levels in clonal plants, (b) the particular spatial structure of their environment, and (c) the importance of clonal plants in different ecological communities.     

Human intestinal microbiota: Role in development and functioning of the nervous system

Recent results related to investigation of the role of intestinal microbiota (IM) in development and functioning of the human nervous system are discussed. The role of the microbiota in bidirectional communication between the gastrointestinal tract and the central nervous system is considered. Special attention is paid to the primary IM of infants, which is actively involved in formation of immune and other physiological mechanisms, including the nervous system, and is responsible for the subsequent general and psychical health of a human. The results of research on ability of the commensal intestinal microflora to produce neuroactive compounds, including neurotransmitters, short- and long-chain fatty acids, γ-aminobutyric acid, etc., are summarized. These compounds may have a considerable effect on development and functioning of the central nervous system, including the brain. Research on various animal models is discussed, including investigation of IM effect on behavior, learning abilities and memory, anxiety and depression levels, reaction to emotional stimuli, and stress resistance. A special section deals with probiotic bacteria, which are presently considered as psychobiotics with preventive and therapeutic potential for treatment of neurological and neurophysiological disorders. Development of new paradigms and concepts, rejection of some classical concepts of neurobiology is presently the key condition for the future breakthrough in investigation of human nervous activity.     

Infrared thermal imaging associated with pain in laboratory animals

The science of animal welfare has evolved over the years, and recent scientific advances have enhanced our comprehension of the neurological, physiological, and ethological mechanisms of diverse animal species. Currently, the study of the affective states (emotions) of nonhuman animals is attracting great scientific interest focused primarily on negative experiences such as pain, fear, and suffering, which animals experience in different stages of their lives or during scientific research. Studies underway today seek to establish methods of evaluation that can accurately measure pain and then develop effective treatments for it, because the techniques available up to now are not sufficiently precise. One innovative technology that has recently been incorporated into veterinary medicine for the specific purpose of studying pain in animals is called infrared thermography (IRT), a technique that works by detecting and measuring levels of thermal radiation at different points on the body’s surface with high sensitivity. Changes in IRT images are associated mainly with blood perfusion, which is modulated by the mechanisms of vasodilatation and vasoconstriction. IRT is an efficient, noninvasive method for evaluating and controlling pain, two critical aspects of animal welfare in biomedical research. The aim of the present review is to compile and analyze studies of infrared thermographic changes associated with pain in laboratory research involving animals.     

Sorting nexin 11 knockout mice exhibit enhanced thermosensing behaviour

Temperature sensing is an important adaptive mechanism for warm‐blooded animals such as humans. ThermoTRP ion channels are activated by distinct but overlapping physiological temperatures. Our previous research demonstrated that sorting nexin 11 (SNX11) regulates lysosomal degradation of plasma membrane TRPV3, one of ThermoTRP ion channel proteins. Here, we found that SNX11, a vesicular trafficking protein, modulates mouse behaviour in response to temperature changes. Snx11‐knockout mice exhibit a stronger preference for mild temperatures along with enhanced sensitivity to harmful heat. Mechanistically, keratinocytes from Snx11‐knockout mice exhibit a larger temperature‐gated TRPV3 membrane current and have enhanced thermoTRPV3 expression in the plasma membrane compared to wild‐type keratinocytes. Additionally, Snx11‐knockout mice show higher endogenous TRPV3 protein levels in skin tissues than wild‐type mice do. Therefore, our results indicate that SNX11 may regulate thermal perception via alteration of functional thermoTRPV3 on the plasma membrane of thermally sensitive cells, which is the first link between vesicular trafficking and thermal transduction.     

Physiological and hormonal control of thermal depression in the tiger snake, Notechis scutatus

Plasma sodium concentrations in field-caught Western tiger snakes, Notechis scutatus, from semi-arid Carnac Island (CI) varied seasonally, with snakes exhibiting significant hypernatraemia during summer and normal concentrations following autumn rain. In contrast, field-caught tiger snakes from a perennial fresh-water swamp (Herdsman Lake, HL) exhibited no significant increase in plasma sodium concentrations during summer. Laboratory-induced hypernatraemia caused thermal depression in both populations; there was a weak negative relationship between plasma sodium concentration and temperature selection that was significant for CI snakes. Hypernatraemia significantly elevated circulating concentrations of the neuropeptide arginine vasotocin (AVT) in both CI and HL snakes. CI snakes injected with a physiological dosage of AVT also evidenced thermal depression. Despite the positive correlation between AVT and both plasma sodium concentration and osmolality for laboratory snakes, field samples from CI snakes indicate that circulating levels of AVT may be influenced more by plasma osmolality than sodium levels. The data suggest that, in CI snakes, chronic dehydration in the field leads to hypernatraemia which may lead to elevated levels of AVT if plasma osmolality also increases. This will in turn invoke a depression in thermal behaviour that may improve the water economy and survival of snakes on semi-arid CI. Although HL snakes do not experience seasonal dehydration, physiological changes away from the stable homeostatic state appear to prompt the same behavioural shifts, illustrating the intrinsic nature of the thermal behaviour in different populations of the same species of snake.     

Physiological Stress in Koala Populations near the Arid Edge of Their Distribution

Recent research has shown that the ecology of stress has hitherto been neglected, but it is in fact an important influence on the distribution and numbers of wild vertebrates. Environmental changes have the potential to cause physiological stress that can affect population dynamics. Detailed information on the influence of environmental variables on glucocorticoid levels (a measure of stress) at the trailing edge of a species’ distribution can highlight stressors that potentially threaten species and thereby help explain how environmental challenges, such as climate change, will affect the survival of these populations. Rainfall determines leaf moisture and/or nutritional content, which in turn impacts on cortisol concentrations. We show that higher faecal cortisol metabolite (FCM) levels in koala populations at the trailing arid edge of their range in southwestern Queensland are associated with lower rainfall levels (especially rainfall from the previous two months), indicating an increase in physiological stress when moisture levels are low. These results show that koalas at the semi-arid, inland edge of their geographic range, will fail to cope with increasing aridity from climate change. The results demonstrate the importance of integrating physiological assessments into ecological studies to identify stressors that have the potential to compromise the long-term survival of threatened species. This finding points to the need for research to link these stressors to demographic decline to ensure a more comprehensive understanding of species’ responses to climate change.     

Seeds of future past: climate change and the thermal memory of plant reproductive traits

Plant persistence and migration in face of climate change depends on successful reproduction by seed, a central aspect of plant life that drives population dynamics, community assembly and species distributions. Plant reproduction by seed is a chain of physiological processes, the rates of which are a function of temperature, and can be modelled using thermal time models. Importantly, while seed reproduction responds to its instantaneous thermal environment, there is also evidence of phenotypic plasticity in response to the thermal history experienced by the plant's recent ancestors, by the reproducing plant since seedling establishment, and by its seeds both before and after their release. This phenotypic plasticity enables a thermal memory of plant reproduction, which allows individuals to acclimatise to their surroundings. This review synthesises current knowledge on the thermal memory of plant reproduction by seed, and highlights its importance for modelling approaches based on physiological thermal time. We performed a comprehensive search in the Web of Science and analysed 533 relevant articles, of which 81 provided material for a meta‐analysis of thermal memory in reproductive functional traits based on the effect size Zr. The articles encompassed the topics of seed development, seed yield (mass and number), seed dormancy (physiological, morphological and physical), germination, and seedling establishment. The results of the meta‐analysis provide evidence for a thermal memory of seed yield, physiological dormancy and germination. Seed mass and physiological dormancy appear to be the central hubs of this memory. We argue for integrating thermal memory into a predictive framework based on physiological time modelling. This will provide a quantitative assessment of plant reproduction, a complex system that integrates past and present thermal inputs to achieve successful reproduction in changing environments. The effects of a warming environment on plant reproduction cannot be reduced to a qualitative interpretation of absolute positives and negatives. Rather, these effects need to be understood in terms of changing rates and thresholds for the physiological process that underlie reproduction by seed.